Publications

Chauhan, M. S., A. Chauhan, M. Bayen, F. Wu, F. A. Althukair, M. T. Kaiser, and L. F. Jacobs, 2024, eNut: A Sensing System to Measure the Acquisition of Foraging Proficiency in Wild Tree Squirrels: IEEE Sensors Journal, v. 24, no. 19, p. 30930–30946, doi:10.1109/jsen.2024.3435834.

We present a three-part sensing system to measure the acquisition of foraging proficiency in wild tree squirrels. The first component is the eNut: a 3-D printed enclosure in the size and shape of a large food item, such as a walnut. The eNut contains an inertial measurement unit (IMU), consisting of an accelerometer and a gyroscope, along with a capsule containing a food reward (e.g., chopped nuts), motivating the squirrel to manipulate the eNut to open the reward capsule. The second component is a radio frequency identification (RFID) gate that can detect the presence of a known individual. The reader generates time-stamped labels for the analysis of simultaneous video recordings of the squirrel movements. Finally, the third component is a data collection pipeline, which aggregates the sensor data in a cloud backend server. The design process culminated in a fully functional prototype system tested under three field conditions: two outdoor sites used for juvenile squirrel rehabilitation and a third site with free-ranging adult squirrels. The accuracy of the collected data is assessed by leveraging laboratory settings in which acceleration and rotation were checked against reference values produced by a testing infrastructure, custom-built for this application. Finally, we present an inventory of food item manipulation movements (rotation and shaking) that are identified and quantified with the eNut system. This system allows a level of granular analyses of foraging decisions that was not feasible with prior technology, which would have important translational value in paradigms of animal behavior and wildlife rehabilitation.

Bratman G N, Bembibre C, Daily G C, Doty R L, Hummel T, Jacobs L F, KahnJr. P H, Lashus C, Majid A, Miller J D, Oleszkiewicz A, Olvera-Alvarez H, Parma V, Riederer A M, Sieber N L, Williams J, Xiao J, Yu C-P and Spengler J D 2024 Nature and human well-being: The olfactory pathway Sci. Adv. 10 10.1126/sciadv.adn3028

The world is undergoing massive atmospheric and ecological change, driving unprecedented challenges to human well-being. Olfaction is a key sensory system through which these impacts occur. The sense of smell influences quality of and satisfaction with life, emotion, emotion regulation, cognitive function, social interactions, dietary choices, stress, and depressive symptoms. Exposures via the olfactory pathway can also lead to (anti-)inflammatory outcomes. Increased understanding is needed regarding the ways in which odorants generated by nature (i.e., natural olfactory environments) affect human well-being. With perspectives from a range of health, social, and natural sciences, we provide an overview of this unique sensory system, four consensus statements regarding olfaction and the environment, and a conceptual framework that integrates the olfactory pathway into an understanding of the effects of natural environments on human well-being. We then discuss how this framework can contribute to better accounting of the impacts of policy and land-use decision-making on natural olfactory environments and, in turn, on planetary health.

Jacobs LF (2023) The PROUST hypothesis: the embodiment of olfactory cognition. Animal Cognition. https://doi.org/10.1007/s10071-022-01734-1

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher’s framework to explore the implications of embodiment for olfactory cognition. The philosopher’s 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent’s cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must therefore begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

Robin AN, Jacobs LF (2022b) The socioeconomics of food hoarding in wild squirrels. Curr Opin Behav Sci 45:101139. https://doi.org/10.1016/j.cobeha.2022.101139

A food-hoarding squirrel reshapes its physical environment through storing food. These changes have ramifications for future economic decisions that cascade into social and reproductive consequences. Food-hoarding strategies exist on a continuum from concentrated caches in a defended larder to scattered caches defended using memory and olfaction. These strategies emerge in response to specific physical environments. Because caches are pilfered, the hoarder must also respond to the competitive social environment. Here, we review recent studies, both from captivity and the field, on the socioeconomics and cognition of hoarding in tree squirrels and chipmunks. As ubiquitous inhabitants of an increasingly urbanized world, these studies illuminate the theoretical and applied research potential of the study of such decisions in squirrels.

Jacobs LF (2022a) How the evolution of air breathing shaped hippocampal function. Philosophical Transactions Royal Soc B 377:20200532. https://doi.org/10.1098/rstb.2020.0532

To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Hunt NH, Jinn J, Jacobs LF, Full RJ (2021) Acrobatic squirrels learn to leap and land on tree branches without falling. Science. https://doi.org/10.1126/science.abe5753

Arboreal animals often leap through complex canopies to travel and avoid predators. Their success at making split-second, potentially life-threatening decisions of biomechanical capability depends on their skillful use of acrobatic maneuvers and learning from past efforts. Here, we found that free-ranging fox squirrels (Sciurus niger) leaping across unfamiliar, simulated branches decided where to launch by balancing a trade-off between gap distance and branch-bending compliance. Squirrels quickly learned to modify impulse generation upon repeated leaps from unfamiliar, compliant beams. A repertoire of agile landing maneuvers enabled targeted leaping without falling. Unanticipated adaptive landing and leaping “parkour” behavior revealed an innovative solution for particularly challenging leaps. Squirrels deciding and learning how to launch and land demonstrates the synergistic roles of biomechanics and cognition in robust gap-crossing strategies.

Jinn J, Connor EG, Jacobs LF (2020) How ambient environment influences olfactory orientation in search and rescue dogs. Chem Senses 45:625–634. https://doi.org/10.1093/chemse/bjaa060

Under natural conditions, an animal orienting to an air-borne odor plume must contend with the shifting influence of meteorological variables, such as air temperature, humidity, and wind speed, on the location and the detectability of the plume. Despite their importance, the natural statistics of such variables are difficult to reproduce in the laboratory and hence few studies have investigated strategies of olfactory orientation by mobile animals under different meteorological conditions. Using trained search and rescue dogs, we quantified the olfactory orientation behaviors of dogs searching for a trail (aged 1–3 h) of a hidden human subject in a natural landscape, under a range of meteorological conditions. Dogs were highly successful in locating the human target hidden 800 m from the start location (93% success). Humidity and air temperature had a significant effect on search strategy: as air conditions became cooler and more humid, dogs searched significantly closer to the experimental trail. Dogs also modified their speed and head position according to their search location distance from the experimental trail. When close to the trail, dogs searched with their head up and ran quickly but when their search took them farther from the trail, they were more likely to search with their nose to the ground, moving more slowly. This study of a mammalian species responding to localized shifts in ambient conditions lays the foundation for future studies of olfactory orientation, and the development of a highly tractable mammalian species for such research.

Jacobs LF (2019) The navigational nose: a new hypothesis for the function of the human external pyramid. J Exp Biol 222:jeb186924. https://doi.org/10.1242/jeb.186924

One of the outstanding questions in evolution is why Homo erectus became the first primate species to evolve the external pyramid, i.e. an external nose. The accepted hypothesis for this trait has been its role in respiration, to warm and humidify air as it is inspired. However, new studies testing the key assumptions of the conditioning hypothesis, such as the importance of turbulence to enhance heat and moisture exchange, have called this hypothesis into question. The human nose has two functions, however, respiration and olfaction. It is thus also possible that the external nose evolved in response to selection for olfaction. The genus Homo had many adaptations for long-distance locomotion, which allowed Homo erectus to greatly expand its species range, from Africa to Asia. Long-distance navigation in birds and other species is often accomplished by orientation to environmental odors. Such olfactory navigation, in turn, is enhanced by stereo olfaction, made possible by the separation of the olfactory sensors. By these principles, the human external nose could have evolved to separate olfactory inputs to enhance stereo olfaction. This could also explain why nose shape later became so variable: as humans became more sedentary in the Neolithic, a decreasing need for long-distance movements could have been replaced by selection for other olfactory functions, such as detecting disease, that would have been critical to survival in newly dense human settlements.

Delgado, M. M, and L. F Jacobs. How squirrels protect their caches: location,
conspicuousness during caching, and proximity to kin influence cache lifespan. BioRxiv 6
(August 16, 2019): 338–45. https://www.biorxiv.org/content/10.1101/738237v1

By genotyping a subpopulation of Berkeley squirrels, Mikel showed that that scatter hoarding fox squirrels placed caches closer to caches made by their close relatives. This suggests that foraging decisions are influenced by kin selection, as the loss of caches to pilfering relatives would be offset by inclusive fitness. Her study also identified key strategic choices squirrels make while caching and how this influences how long the cache remains hidden before it is retrieved or pilfered.

Delgado, M.M. & Jacobs, L.F., 2017. Caching for where and what: evidence for a mnemonic strategy in a scatter-hoarder. Royal Society Open Science, 4(9), pp.170958–6.

Squirrels organize their caches spatially by the species of nut. Such ‘spatial chunking’ increases the accuracy of memory recall in other species and probably reduces the cognitive load of building and managing an optimal cache map.

Delgado, M.M. and Jacobs, L.F. (2016). Inaccessibility of reinforcement increases persistence and signaling behavior in the fox squirrel, Sciurus niger. Journal of Comparative Psychology. 130(2): 128-137.

Is frustration adaptive? See the experiment here in this short film by KQED http://”Watch Those Frustrated Squirrels”

Jacobs, L. F., Arter, J., Cook, A., & Sulloway, F. J. (2015). Olfactory orientation and navigation in humans. PLoS ONE, 10(6), e0129387. http://doi.org/10.1371/journal.pone.0129387.s001

Although predicted by theory, there is no direct evidence that an animal can define an arbitrary location in space as a coordinate location on an odor grid. Here we show that humans can do so. Using a spatial match-to-sample procedure, humans were led to a random location within a room diffused with two odors. After brief sampling and spatial disorientation, they had to return to this location. Over three conditions, participants had access to different sensory stimuli: olfactory only, visual only, and a final control condition with no olfactory, visual, or auditory stimuli. Humans located the target with higher accuracy in the olfactiononly condition than in the control condition and showed higher accuracy than chance. Thus a mechanism long proposed for the homing pigeon, the ability to define a location on a map constructed from chemical stimuli, may also be a navigational mechanism used by humans.

Jacobs, L. F., & Menzel, R. (2014). Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab. Movement Ecology, 2(1), 1–22. http://doi.org/10.1186/2051-3933-2-3

Space is continuous. But the communities of researchers that study the cognitive map in non-humans are strangely divided, with debate over its existence found among behaviorists but not neuroscientists. To reconcile this and other debates within the field of navigation, we return to the concept of the parallel map theory, derived from data on hippocampal function in laboratory rodents. Here the cognitive map is redefined as the integrated map, which is a construction of dual mechanisms, one based on directional cues (bearing map) and the other on positional cues (sketch map). We propose that the dual navigational mechanisms of pigeons, the navigational map and the familiar area map, could be homologous to these mammalian parallel maps; this has implications for both research paradigms. Moreover, this has implications for the lab. To create a bearing map (and hence integrated map) from extended cues requires self-movement over a large enough space to sample and model these cues at a high resolution. Thus a navigator must be able to move freely to map extended cues; only then should the weighted hierarchy of available navigation mechanisms shift in favor of the integrated map. Because of the paucity of extended cues in the lab, the flexible solutions allowed by the integrated map should be rare, despite abundant neurophysiological evidence for the existence of the machinery needed to encode and map extended cues through voluntary movement. Not only do animals need to map extended cues but they must also have sufficient information processing capacity. This may require a specific ontogeny, in which the navigator’s nervous system is exposed to naturally complex spatial contingencies, a circumstance that occurs rarely, if ever, in the lab. For example, free-ranging, flying animals must process more extended cues than walking animals and for this reason alone, the integrated map strategy may be found more reliably in some species. By taking concepts from ethology and the parallel map theory, we propose a path to directly integrating the three great experimental paradigms of navigation: the honeybee, the homing pigeon and the laboratory rodent, towards the goal of a robust, unified theory of animal navigation.

Delgado, M. M., Nicholas, M., Petrie, D. J., & Jacobs, L. F. (2014). Fox squirrels match food assessment and cache effort to value and scarcity. PLoS ONE, 9(3), e92892. http://doi.org/10.1371/journal.pone.0092892.s003

Scatter hoarders must allocate time to assess items for caching, and to carry and bury each cache. Such decisions should be driven by economic variables, such as the value of the individual food items, the scarcity of these items, competition for food items and risk of pilferage by conspecifics. The fox squirrel, an obligate scatter-hoarder, assesses cacheable food items using two overt movements, head flicks and paw manipulations. These behaviors allow an examination of squirrel decision processes when storing food for winter survival. We measured wild squirrels’ time allocations and frequencies of assessment and investment behaviors during periods of food scarcity (summer) and abundance (fall), giving the squirrels a series of 15 items (alternating five hazelnuts and five peanuts). Assessment and investment per cache increased when resource value was higher (hazelnuts) or resources were scarcer (summer), but decreased as scarcity declined (end of sessions). This is the first study to show that assessment behaviors change in response to factors that indicate daily and seasonal resource abundance, and that these factors may interact in complex ways to affect food storing decisions. Food-storing tree squirrels may be a useful and important model species to understand the complex economic decisions made under natural conditions.

Evan L. MacLean, Brian A. Hare, Charles L. Nunn, Elsa Addessi, Federica Amici, Rindy C. Anderson, Filippo Aureli, Joseph M. Baker, Amanda E. Bania, Allison M. Barnard, Neeltje J. Boogert, Elizabeth M. Brannon, Emily E. Bray, Joel Bray, Lauren J. N. Brent, Judith M. Burkart, Josep Call, Jessica F. Cantlon, Lucy G. Cheke, Nicola S. Clayton, Mikel M. Delgado, Louis J. DiVincenti, Kazuo Fujita, Chihiro Hiramatsu, Lucia F. Jacobs, Kerry E. Jordan, Jennifer R. Laude, Kristin L. Leimgruber, Emily J. E. Messer, Antonio C. de A. Moura, Ljerka Ostojić, Alejandra Picard, Michael L. Platt, Joshua M. Plotnik, Friederike Range, Simon M. Reader, Rachna B. Reddy, Aaron A. Sandel, Laurie R. Santos, Katrin Schumann, Amanda M. Seed, Kendra B. Sewall, Rachael C. Shaw, Katie E Slocombe, Yanjie Su, Ayaka Takimoto, Jingzhi Tan, Ruoting Tao, Carel P. van Schaik, Zsófia Virányi, Elisabetta Visalberghi, Jordan C. Wade, Arii Watanabe, Jane Widness, Thomas R. Zentall, Yini Zhao. (2014) The evolution of self-control. Proceedings of the National Academy of Sciences, 111(20), E2140–8. doi:10.1073/pnas.1323533111.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Bettis TJ, Jacobs LF (2013) Sex differences in memory for landmark arrays in C57BL/J6 mice. Animal Cognition 16:873–882. https://doi.org/10.1007/s10071-013-0619-x

Cook, A., Arter, J., & Jacobs, L. F. (2013). My owner, right or wrong: the effect of familiarity on the domestic dog’s behavior in a food-choice task. Animal Cognition, 17(2), 461–470. http://doi.org/10.1007/s10071-013-0677-0

Waismeyer, A. S., & Jacobs, L. F. (2013). The emergence of flexible spatial strategies in young children. Developmental Psychology, 49(2), 232–242. http://doi.org/10.1037/a0028334

Jacobs, L. F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci, 109, 10693–10700. http://doi.org/10.1073/pnas.1201880109

Bettis, T., & Jacobs, L. F. (2012). Sex differences in object recognition are modulated by object similarity. Behavioural Brain Research, 233(2), 288–292. http://doi.org/10.1016/j.bbr.2012.04.028

Chai, X. J., & Jacobs, L. F. (2012). Digit ratio predicts sense of direction in women. PLoS ONE, 7(2), e32816. http://doi.org/10.1371/journal.pone.0032816

Kleschevnikov, A. M., Belichenko, P. V., Faizi, M., Jacobs, L. F., Htun, K., Shamloo, M., & Mobley, W. C. (2012). Deficits in cognition and synaptic plasticity in a mouse model of Down Syndrome ameliorated by GABAB receptor antagonists. Journal of Neuroscience, 32(27), 9217–9227. http://doi.org/10.1523/JNEUROSCI.1673-12.2012

MacLean, E.L., Matthews, L.J., Hare, B.A., Nunn, C.L., Anderson, R.C., Aureli, F., Brannon, E.M., Call, J., Drea, C.M., Emery, N.J., Haun, D.B., Herrmann, E., Jacobs, L.F., Platt, M.L., Rosati, A.G., Sandel, A.A., Schroepfer, K.K., Seed, A.M., Tan, J., van Schaik, C.P., and Wobber, V. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition 15, 223-238. https://doi.org/10.1007/s10071-011-0448-8.

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Wiener, J., Shettleworth, S., Bingman, V.P., Cheng, K., Healy, S., Jacobs, L.F., Jeffery, K.J., Mallot, H.A., Menzel, R., and Newcombe, N.S. (2011). Animal Navigation – A Synthesis. In Animal Thinking: Contemporary Issues in Comparative Cognition, R. Menzel, and J. Fischer, eds. (Cambridge, MA, MIT Press).

Waisman, A. S., Lucas, C. G., Griffiths, T. L., & Jacobs, L. F. (2011). A Bayesian model of navigation in squirrels. Presented at the Proc 33rd Annual Conf Cog Sci Society.

Chai, X. J., & Jacobs, L. F. (2010). Effects of cue types on sex differences in human spatial memory. Behavioural Brain Research, 208(2), 336–342. http://doi.org/10.1016/j.bbr.2009.11.039

Chai, X. J., Ofen, N., Jacobs, L. F., & Gabrieli, J. D. E. (2010). Scene complexity: influence on perception, memory, and development in the medial temporal lobe. Frontiers in Human Neuroscience, 4, 21–10. http://doi.org/10.3389/fnhum.2010.00021

Chai, X. J., & Jacobs, L. F. (2009). Sex differences in directional cue use in a virtual landscape. Behavioral Neuroscience, 123(2), 276–283. http://doi.org/10.1037/a0014722

Bettis, T. J., & Jacobs, L. F. (2009). Sex-specific strategies in spatial orientation in C57BL/6J mice. Behavioural Processes.

Preston SD, Jacobs LF (2009) Mechanisms of cache decision making in fox squirrels (Sciurus niger). J Mammal 90:787–795. https://doi.org/10.1644/08-mamm-a-254.1

The cache decisions of scatter-hoarding animals are influenced by a number of factors, including satiety, food quality, number of competitors, and the risk of predation and pilferage. However, it is unknown how animals assess these variables. We investigated this process experimentally in free-ranging fox squirrels (Sciurus niger) by measuring the effects of nut characteristics and social context on nut-handling behavior and subsequent cache decisions. We found that a behavior involved in nut handling, the head flick, was correlated with nut quality, shell presence, the decision to cache rather than eat the nut, and the time and energy spent caching. In contrast, a 2nd nut-handling behavior, the paw maneuver, was correlated with the social context but not the cache decision, and may instead reflect a response to social competition. Our results suggest that fox squirrels assess nut quality using overt, observable nut-handling behaviors. The experimental study of these behaviors can help us understand how animals use information about food and the social context to make adaptive food-storing decisions.

Jacobs, L. F. (2009). The role of social selection in the evolution of hippocampal specialization. In L. Tommasi, M. A. Peterson, & L. Nadel (Eds.), Cognitive Biology: Evolutionary and Developmental Perspectives on Mind. Cambridge, MA: MIT Press.

Waisman AS, Jacobs LF (2008) Flexibility of cue use in the fox squirrel (Sciurus niger). Anim Cogn 11:625–636. https://doi.org/10.1007/s10071-008-0152-5

Recent work on captive flying squirrels has demonstrated a novel degree of flexibility in the use of different orientation cues. In the present study, we examine to what extent this flexibility is present in a free-ranging population of another tree squirrel species, the fox squirrel. We trained squirrels to a rewarded location within a square array of four feeders and then tested them on transformations of the array that either pitted two cue types against one cue type, the majority tests, or all cue types against each other, the forced-hierarchy test. In Experiment 1, squirrels reoriented to the two-cue-type location in all majority tests and to the location indicated by the visual features of the feeders in the forced-hierarchy test. This preference for visual features runs contrary to previous studies that report the use of spatial cues over visual features in food-storing species. In Experiments 2–5 we tested squirrels with different trial orders (Experiments 2 and 3), a different apparatus (Experiment 4) and at different times of the year (Experiment 5) to determine why these squirrels had chosen to orient using visual features in the first experiment. Like captive flying squirrels, free-ranging fox squirrels showed a large degree of flexibility in their use of cues. Furthermore, their cue use appeared to be sensitive both to changes in the test apparatus and the season in which we tested. Altogether our results suggest that the study of free-ranging animals over a variety of conditions is necessary for understanding spatial cognition.

Barkley, C., & Jacobs, L. F. (2007). Sex and species differences in spatial memory in food-storing kangaroo rats. Animal Behaviour, 73(2), 321–329. http://doi.org/10.1016/j.anbehav.2006.07.009

Scatter-hoarding birds show superior performance in many spatial memory tasks and appear to relocate sites using different cues than nonscatter hoarders. However, there have not been similar studies of cue use and memory for locations by mammals that differ in their reliance on scatter hoards for survival. Here we report differences in spatial memory in two species of kangaroo rats that are predicted by foraging ecology. Merriam’s kangaroo rat, Dipodomys merriami, a scatter hoarder that hoards intensively, showed accurate memory on a cache simulation task, which required the rat to find four predetermined locations after a 24-h delay. In contrast, the leaf-eating specialist Great Basin kangaroo rat, D. microps, which relies less on scatter hoarding, showed poorer accuracy under the same experimental conditions. The presence of local landmarks did not differentially affect recovery in the two species of kangaroo rats, unlike previous studies in birds. We did find a significant interaction between the presence of local landmarks and sex on target recovery. Female performance was significantly impaired by the absence of local landmarks, while male performance was unaltered. Spatial ecology predicted both species and sex differences in spatial memory in kangaroo rats.

Gibbs SEB, Lea SEG, Jacobs LF (2007) Flexible use of spatial cues in the southern flying squirrel (Glaucomys volans). Anim Cogn 10:203–209. https://doi.org/10.1007/s10071-006-0059-y

Insects, birds, and mammals have been shown capable of encoding spatial information in memory using multiple strategies or frames of reference simultaneously. These strategies include orientation to a goal-specific cue or beacon, to the position of the goal in an array of local landmarks, or to its position in the array of distant landmarks, also known as the global frame of reference. From previous experiments, it appears that birds and mammals that scatter hoard rely primarily on a global frame of reference, but this generalization depends on evidence from only a few species. Here we examined spatial memory in a previously unstudied scatter hoarder, the southern flying squirrel. We dissociated the relative weighting of three potential spatial strategies (beacon, global, or relative array strategy) with three probe tests: transposition of beacon and the rotation or the expansion of the array. The squirrels’ choices were consistent with a spatial averaging strategy, where they chose the location dictated by at least two of the three strategies, rather than using a single preferred frame of reference. This adaptive and flexible heuristic has not been previously described in animal orientation studies, yet it may be a common solution to the universal problem of encoding and recalling spatial locations in an ephemeral physical landscape.

Adams-Hunt, Melissa M., and Jacobs, Lucia F. (2007). Learning to forage. In: Foraging: Behavior and Ecology, D.W. Stephens, J.S. Brown, and R.C. Ydenberg, eds. (Chicago, IL, University of Chicago), p. 576.

Jacobs, L. F. (2006). From movement to transitivity: the role of hippocampal parallel maps in configural learning. Reviews in the Neurosciences, 17(1-2), 99–109.

Whether spatial learning is a special case of configural or relational learning, or whether abstract principles evolved from the concrete need to navigate in space, is a question of long-standing debate. The parallel map theory of hippocampal function offers a resolution of the debate by redefining ‘spatial learning’ as two parallel, geometric processes, Euclidean metric and topological. Moreover, these processes are subserved by independent hippocampal subfields that underlie two ways of representing space, the bearing and the sketch map. It is possible that configural and relational learning, like spatial learning, should also be distinguished in this way. Transitive inference, requiring the construction of a value gradient, could be analyzed as a Euclidean metric problem. In contrast, transverse patterning could be seen as a topological analysis of the relationships among discrete objects. If this interpretation is correct, lesions to the primary bearing map structure (dentate gyrus) should impair transitivity while lesions to the primary sketch map structure (CA1) should impair transverse patterning and similar topological tasks. Recent results from diverse species and tasks lend support to these predictions, suggesting that the hippocampus not only creates parallel maps but uses these maps to solve more abstract configural or relational problems.

Hermes, G. L., Jacobs, L. F., & McClintock, M. (2005). The sectored foraging field: A novel design to quantify spatial strategies, learning, memory, and emotion. Neurobiology of Learning and Memory, 84(1), 69–73.

Preston SD, Jacobs LF (2005) Cache decision making: The effects of competition on cache decisions in Merriam’s Kangaroo Rat (Dipodomys merriami). J Comp Psychol 119:187–196. https://doi.org/10.1037/0735-7036.119.2.187

Caching food is an economic, decision-making process that requires animals to take many factors into account, including the risk of pilferage. However, little is known about how food-storing animals determine the risk of pilferage. In this study, the authors examined the effect of a dominant competitor species on the caching and behavior of Merriam’s kangaroo rat (Dipodomys merriami). The authors found that, as with conspecific competitors, kangaroo rats did not alter caching in response to the mere presence of a heterospecific competitor, but moved caches to an unpreferred area when the competitor’s presence was paired with pilferage. These data suggest that Merriam’s kangaroo rat assesses pilfer risk from actual pilferage by a competitor and adaptively alters cache strategy to minimize future risk.

Jacobs, L. F., & Schenk, F. (2003). Unpacking the cognitive map: the parallel map theory of hippocampal function. Psychological Review, 110(2), 285–315.

In the parallel map theory, the hippocampus encodes space with 2 mapping systems. The bearing map is constructed primarily in the dentate gyrus from directional cues such as stimulus gradients. The sketch map is constructed within the hippocampus proper from positional cues. The integrated map emerges when data from the bearing and sketch maps are combined. Because the component maps work in parallel, the impairment of one can reveal residual learning by the other. Such parallel function may explain paradoxes of spatial learning, such as learning after partial hippocampal lesions, taxonomic and sex differences in spatial learning, and the function of hippocampal neurogenesis. By integrating evidence from physiology to phylogeny, the parallel map theory offers a unified explanation for hippocampal function.

Jacobs, L. F. (2003). The evolution of the cognitive map. Brain, Behavior and Evolution, 62(2), 128–139. http://doi.org/10.1159/000072443

The hippocampal formation of mammals and birds mediates spatial orientation behaviors consistent with a map-like representation, which allows the navigator to construct a new route across unfamiliar terrain. This cognitive map thus appears to underlie long-distance navigation. Its mediation by the hippocampal formation and its presence in birds and mammals suggests that at least one function of the ancestral medial pallium was spatial navigation. Recent studies of the goldfish and certain reptile species have shown that the medial pallium homologue in these species can also play an important role in spatial orientation. It is not yet clear, however, whether one type of cognitive map is found in these groups or indeed in all vertebrates. To answer this question, we need a more precise definition of the map. The recently proposed parallel map theory of hippocampal function provides a new perspective on this question, by unpacking the mammalian cognitive map into two dissociable mapping processes, mediated by different hippocampal subfields. If the cognitive map of non-mammals is constructed in a similar manner, the parallel map theory may facilitate the analysis of homologies, both in behavior and in the function of medial pallium subareas.

Preston, S. D., & Jacobs, L. F. (2001). Conspecific pilferage but not presence affects Merriam’s kangaroo rat cache strategy. Behavioral Ecology, 12(5), 517–523.

We investigated the effects of pilferage on caching behavior in the Merriam’s kangaroo rat by manipulating two factors associated with pilferage: the presence of a conspecific, and the opportunity for pilferage. In one experiment we assessed animals in either ‘‘Stealer’’ or ‘‘Victim’’ roles and measured changes in caching, space use, and behavior after caches were pilfered. Victims shifted from a majority scatter-hoarding to a majority larder-hoarding strategy after their caches were pilfered by the Stealer. In Experiment 2, we measured changes after exposure to a conspecific when there was no pilferage, with or without prior exposure to pilferage from Experiment 1. Merriam’s kangaroo rats were vigilant when a conspecific was present, but did not change cache strategy. Prior exposure did not have any major effect on caching or behavior. Food storage is an economic decision that is often made by a solitary forager. Our results suggest that social competition nonetheless influences such economic decisions, even in a nonsocial forager.

Jacobs, L.F. (2000). Sexual differentiation and cognitive function. In: Gender and Society: the 1995 Herbert Spencer Lectures, S. Iversen, ed. (Oxford, UK, Oxford University Press).

Lavenex, P., Steele, M. A., & Jacobs, L. F. (2000). Sex differences, but no seasonal variations in the hippocampus of food‐caching squirrels: A stereological study. Journal of Comparative Neurology, 425(1), 152–166.

Lavenex, P., Steele, M. A., & Jacobs, L. F. (2000). The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. European Journal of Neuroscience, 12(2), 643–648.

Jacobs, L. F., & Shiflett, M. W. (1999). Spatial orientation on a vertical maze in free-ranging fox squirrels ( Sciurus niger). Journal of Comparative Psychology, 113(2), 116–127.

To determine how squirrels return to remembered locations in an arboreal environment, wild fox squirrels (Sciurus niger) were trained on an outdoor vertical maze. Squirrels were trained on 1 route and tested with all routes accessible. Possible mechanisms of spatial orientation were distinguished with manipulations such as rotations, shifts, and blocked routes. Squirrels consistently used an extra-maze, allothetic frame of reference to orient and appeared to organize their memory of the route hierarchically. This study demonstrates that a laboratory technique, the maze, can be successfully brought into the field to measure mechanisms of spatial orientation under natural conditions in free-ranging wild rodents. Such studies will allow researchers to determine what kind of spatial information is acquired by wild animals under natural conditions and how this information is used.

Barkley, C., & Jacobs, L. F. (1998). Visual environment and delay affect cache retrieval accuracy in a food-storing rodent. Learning & Behavior, 26(4), 439–447.

Many scatter-hoarding species use spatial memory to relocate their food caches. Two factors can affect spatial memory: the availability of landmarks in the environment, and the latency between learning and recall. Using a 2 × 2 factorial design, we determined the effect of these factors on cache retrieval accuracy in Merriam’s kangaroo rats (Dipodomys merriami). Kangaroo rats cached seeds in an arena under conditions that varied by retrieval interval (1 or 10 days) and by number of landmarks (0 or 16 landmarks). After 1 day, they recovered equal proportions of caches in both landmark conditions. After 10 days, they recovered more caches in the 16-landmark condition than in the bare condition. This is the first study to show that landmarks are necessary for accurate cache recovery after long delays. This result is consistent with maze studies that have shown that landmarks reduce proactive interference and that delay increases proactive interference.

Lavenex, P., Shiflett, M. W., Lee, R. K., & Jacobs, L. F. (1998). Spatial versus nonspatial relational learning in free-ranging fox squirrels (Sciurus niger). Journal of Comparative Psychology, 112(2), 127–136.

Feener, D. H., Jacobs, L. F., & Schmidt, J. O. (1996). Specialized parasitoid attracted to a pheromone of ants. Animal Behaviour, 51(1), 61–66.

Jacobs, L. F. (1996). Sexual selection and the brain. Trends Ecol Evol, 11(2), 82–86.

Sex differences are intrinsically interesting, particularly in the brain. When sexually dimorphic structures mediate learning, and when such learning ability is necessary to compete for mates, then such differences are best understood within the framework of sexual selection. By categorizing recent studies of sex differences in the brain by their role in mate competition, theories of sexual selection can be used to predict and characterize the occurrence of dimorphisms among species with different mating systems.

Jacobs, L. F. (1996). The economy of winter: phenotypic plasticity in behavior and brain structure. The Biological Bulletin, 191(1), 92–100. https://doi.org/10.2307/1543068

Mobile animals must learn the spatial distributions of resources. The cost of foraging increases dramatically for temperate-zone animals during the winter. Two strategies may be used to balance the energetic budget: reducing costs of foraging and reducing need to forage. Both strategies are correlated with changes in brain structure, specifically in the hippocampus, a fore-brain structure used by birds and mammals to map spatial distributions of resources. Small mammals that reduce their need to forage, through hibernation or reduction in body size, show a specific reduction in the structure and size of the hippocampus. The costs of foraging can be also decreased by migration to better foraging conditions or by food-storing, both of which decrease the temporal heterogeneity of food resources. Both of these latter strategies are associated with increased hippocampal structure; for food-storing birds, this increase is a seasonal phenomenon. Thus not only behavior, but also learning ability and even brain structures in adult animals, may be phenotypically plastic in response to the changing demands of the environment.

Jacobs, L. F. (1995). The ecology of spatial cognition: adaptive patterns of hippocampal size and space use in wild rodents. In E. Alleva, A. Fasolo, H.-P. Lipp, & L. Nadel (Eds.), (pp. 301–322). Dordrecht: Behavioural Brain Research in Naturalistic and Semi-Naturalistic Setting.

Jacobs, L. F., & Spencer, W. D. (1994). Natural space-use patterns and hippocampal size in kangaroo rats. Brain, Behavior and Evolution, 44(3), 125–132.

The size of the hippocampus, a forebrain structure that processes spatial information, correlates with the need to relocate food caches by passerine birds and with sex-specific patterns of space use in microtine rodents. The influences on hippocampal anatomy of sexual selection within species, and natural selection between species, have not yet been studied in concert, however. Here we report that natural space-use patterns predict hippocampal size within and between two species of kangaroo rats (Dipodomys). Differences in foraging behavior suggest that Merriam”s kangaroo rats (D. merriami) require better spatial abilities than bannertail kangaroo rats (D. spectabilis). Sex-specific differences in mating strategy suggest that males of both species require more spatial ability than females. As predicted, hippocampal size (relative to brain size) is larger in Merriam”s than in bannertail kangaroo rats, and males have larger hippocampi than females in both species. Males of a third species (D. ordii) also have smaller hippocampi than Merriam’s kangaroo rat males, despite being similar to Merriam”s in brain and body size. These results suggest that both natural and sexual selection affect the relative size and perhaps function of mammalian hippocampi. They also reassert that measures of functional subunits of the brain reveal more about brain evolution than measures of total brain size.

Daly, M., Behrends, P., Wilson, M. I., & Jacobs, L. F. (1992). Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Animal Behaviour, 44(1), 1–9.

Collaboration with Margo Wilson and Martin Daly

Daly M, Jacobs LF, Wilson MI, Behrends PR (1992) Scatter hoarding by kangaroo rats (Dipodomys merriami) and pilferage from their caches. Behav Ecol 3:102–111. https://doi.org/10.1093/beheco/3.2.102

Collaboration with Margo Wilson and Martin Daly

We observed radio-implanted Merriam’s kangaroo rats disposing of 10-g bonanzas of rolled oats in 48 trials in the field. The principal determinant of the initial disposition of discovered food was apparently its distance from the day burrow: food found within about 10m was mainly larder hoarded, whereas food encountered farther afield was usually dispersed immediately in shallow caches. Cache sites were newly dug for the purpose and not reused; most caches were nearer the current day burrow than was the food source, but a few were placed far from both the cacher’s day burrow and its habitual nocturnal range. An experiment with artificial caches indicated that security from discovery increases with spacing and with proximity to perennial shrubs. Nine kangaroo rats cached dyed food, and fecal dye traces revealed extensive pilferage from five of them, by both conspecifics and other rodent species. Limited evidence indicates that food encountered nearer home and initially larder hoarded was more secure from pilferage than food initially scattered, and yet kangaroo rats were observed to scatter caches soon after initial larder hoarding. A kangaroo rat whose dyed stores escaped pilferage fed from them at intervals for at least 12 days. Even cachers who incurred pilferage made as much, or more, use of their caches as any thief, suggesting that scattering caches may be a defense against catastrophic losses.

Daly, M., Wilson, M. I., Behrends, P., & Jacobs, L. F. (1992). Sexually differentiated effects of radio transmitters on predation risk and behaviour in kangaroo rats (Dipodomys merriami). Canadian Journal of Zoology, 70(9), 1851–1855.

Jacobs LF (1992) Memory for cache locations in Merriam’s kangaroo rats. Animal Behaviour 43:585–593. https://doi.org/10.1016/0003-3472(92)90081-j

The ability of Merriam’s kangaroo rats, Dipodono’s merriami, to remember the location of food caches and to relocate caches in the absence of the odour of buried seeds was examined. Eight wild-caught kangaroo rats cached seeds in an experimental arena, and retrieved them 24 h later. Before retrieval, all odours associated with the cache sites were removed and seeds were replaced in only halfofthe cache sites. During retrieval, kangaroo rats were significantly more likely to search cache sites, with or without seeds, than non-cache sites. Non-cache sites were primarily investigated after all cache sites had been searched, indicating that search of non-cache sites did not denote an error in cache retrieval. These results suggest that kangaroo rats can remember the locations of food caches, and can relocate cache sites even when there is no odour of buried seeds. To estimate the advantage enjoyed by the forager with greater information, a second experiment compared an owner’s success in retrieving its caches with the success of naive kangaroo rats searching for these same caches. Nine wild-caught kangaroo rats were allowed to search for caches that were distributed in the same spatial pattern as that created by one kangaroo rat from the first experiment. The naive subjects found significantly fewer caches than had the cache owner in the same length of time. This suggests that the use of spatial memory by a Merriam’s kangaroo rat to relocate its food caches gives it a competitive advantage over other kangaroo rats that may be searching for its caches.

Jacobs LF (1992) The effect of handling time on the decision to cache by grey squirrels. Anim Behav 43:522–524. https://doi.org/10.1016/s0003-3472(05)80111-3

Sherry DF, Jacobs LF, Gaulin SJC (1992) Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298–303. https://doi.org/10.1016/0166-2236(92)90080-r

The hippocampus plays an important role in spatial memory and spatial cognition in birds and mammals. Natural selection, sexual selection and artificial selection have resulted in an increase in the size of the hippocampus in a remarkably diverse group of animals that rely on spatial abilities to solve ecologically important problems. Food-storing birds remember the locations of large numbers of scattered caches. Polygynous male voles traverse large home ranges in search of mates. Kangaroo rats both cache food and exhibit a sex difference in home range size. In all of these species, an increase in the size of the hippocampus is associated with superior spatial ability. Artificial selection for homing ability has produced a comparable increase in the size of the hippocampus in homing pigeons, compared with other strains of domestic pigeon. Despite differences among these animals in their histories of selection and the genetic backgrounds on which selection has acted, there is a common relationship between relative hippocampal size and spatial ability.

Jacobs LF, Liman Emily R. (1991) Grey squirrels remember the locations of buried nuts. Anim Behav 41:103–110. https://doi.org/10.1016/s0003-3472(05)80506-8

It has previously been assumed that grey squirrels, Sciurus carolinensis, cannot remember the locations of nuts they have buried, and hence must relocate nuts by their odour. This assumption was tested by measuring the accuracy of cache retrieval of captive squirrels. Each squirrel was released alone into an outdoor arena, where it cached 10 hazelnuts. After a delay of 2,4 or 12 days, each squirrel was returned to the arena and tested for its ability to retreve nuts from its own cache sites and from 10 cache sites used by other squirrels. Although each squirrel’s own caches were close to the caches of other squirrels, the squirrels retrieved significantly more nuts from their own sites than from sites used by other squirrels, after all delays. The retrieval accuracy of the squirrels under these conditions indicates that while grey squirrels can locate buried nuts by their odour, they can also remember the individual locations of nuts they have buried.

Jacobs LF, Gaulin SJ, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc National Acad Sci 87:6349–6352. https://doi.org/10.1073/pnas.87.16.6349

In a study of two congeneric rodent species, sex differences in hippocampal size were predicted by sex-specific patterns of spatial cognition. Hippocampal size is known to correlate positively with maze performance in laboratory mouse strains and with selective pressure for spatial memory among passerine bird species. In polygamous vole species (Rodentia: Microtus), males range more widely than females in the field and perform better on laboratory measures of spatial ability; both of these differences are absent in monogamous vole species. Ten females and males were taken from natural populations of two vole species, the polygamous meadow vole, M. pennsylvanicus, and the monogamous pine vole, M. pinetorum. Only in the polygamous species do males have larger hippocampi relative to the entire brain than do females. Two-way analysis of variance shows that the ratio of hippocampal volume to brain volume is differently related to sex in these two species. To our knowledge, no previous studies of hippocampal size have linked both evolutionary and psychometric data to hippocampal dimensions. Our controlled comparison suggests that evolution can produce adaptive sex differences in behavior and its neural substrate.

Daly M, Wilson M, Behrends PR, Jacobs LF (1990) Characteristics of kangaroo rats, Dipodomys merriami, associated with differential predation risk. Anim Behav 40:380–389. https://doi.org/10.1016/s0003-3472(05)80934-0.

Between 1980 and 1990, 176 adult Merriam’s kangaroo rats were subcutaneously implanted with radio transmitters and tracked for a total of 6316 animal-days at a California site, prior to and during reproductive seasons. Thirty-six animals are known to have been killed by predators, and 14 who disappeared abruptly are also presumed victims. These 50 cases permit various analyses of differential predation risk. Males incurred a predation rate (4·22 deaths per animal-year) more than twice that of females (2·01); this sex difference in mortality was apparently absent or reversed after the breeding season. Both male and female victims travelled significantly greater distances between successive radio-locations shortly before their deaths than surviving same-sex animals tracked contemporaneously. Rather than being selective for the feeble, predation on kangaroo rats is selective for the mobile.

Sengelaub, D. R., Jacobs, L. F., & Finlay, B. L. (1985). Regional differences in normally occurring cell death in the developing hamster lateral geniculate nuclei. Neuroscience Letters, 55(2), 103–108.

Jacobs LF (2023) The PROUST hypothesis: the embodiment of olfactory cognition. Animal Cognition. https://doi.org/10.1007/s10071-022-01734-1

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher’s framework to explore the implications of embodiment for olfactory cognition. The philosopher’s 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent’s cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must therefore begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

Jacobs LF (2023) The PROUST hypothesis: the embodiment of olfactory cognition. Animal Cognition. https://doi.org/10.1007/s10071-022-01734-1

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher’s framework to explore the implications of embodiment for olfactory cognition. The philosopher’s 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent’s cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must therefore begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

Jacobs LF (2023) The PROUST hypothesis: the embodiment of olfactory cognition. Animal Cognition. https://doi.org/10.1007/s10071-022-01734-1

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher’s framework to explore the implications of embodiment for olfactory cognition. The philosopher’s 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent’s cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must therefore begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

Robin AN, Jacobs LF (2022b) The socioeconomics of food hoarding in wild squirrels. Curr Opin Behav Sci 45:101139. https://doi.org/10.1016/j.cobeha.2022.101139

A food-hoarding squirrel reshapes its physical environment through storing food. These changes have ramifications for future economic decisions that cascade into social and reproductive consequences. Food-hoarding strategies exist on a continuum from concentrated caches in a defended larder to scattered caches defended using memory and olfaction. These strategies emerge in response to specific physical environments. Because caches are pilfered, the hoarder must also respond to the competitive social environment. Here, we review recent studies, both from captivity and the field, on the socioeconomics and cognition of hoarding in tree squirrels and chipmunks. As ubiquitous inhabitants of an increasingly urbanized world, these studies illuminate the theoretical and applied research potential of the study of such decisions in squirrels.

Jacobs LF (2022a) How the evolution of air breathing shaped hippocampal function. Philosophical Transactions Royal Soc B 377:20200532. https://doi.org/10.1098/rstb.2020.0532

To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Hunt NH, Jinn J, Jacobs LF, Full RJ (2021) Acrobatic squirrels learn to leap and land on tree branches without falling. Science. https://doi.org/10.1126/science.abe5753

Arboreal animals often leap through complex canopies to travel and avoid predators. Their success at making split-second, potentially life-threatening decisions of biomechanical capability depends on their skillful use of acrobatic maneuvers and learning from past efforts. Here, we found that free-ranging fox squirrels (Sciurus niger) leaping across unfamiliar, simulated branches decided where to launch by balancing a trade-off between gap distance and branch-bending compliance. Squirrels quickly learned to modify impulse generation upon repeated leaps from unfamiliar, compliant beams. A repertoire of agile landing maneuvers enabled targeted leaping without falling. Unanticipated adaptive landing and leaping “parkour” behavior revealed an innovative solution for particularly challenging leaps. Squirrels deciding and learning how to launch and land demonstrates the synergistic roles of biomechanics and cognition in robust gap-crossing strategies.

Jinn J, Connor EG, Jacobs LF (2020) How ambient environment influences olfactory orientation in search and rescue dogs. Chem Senses 45:625–634. https://doi.org/10.1093/chemse/bjaa060

Under natural conditions, an animal orienting to an air-borne odor plume must contend with the shifting influence of meteorological variables, such as air temperature, humidity, and wind speed, on the location and the detectability of the plume. Despite their importance, the natural statistics of such variables are difficult to reproduce in the laboratory and hence few studies have investigated strategies of olfactory orientation by mobile animals under different meteorological conditions. Using trained search and rescue dogs, we quantified the olfactory orientation behaviors of dogs searching for a trail (aged 1–3 h) of a hidden human subject in a natural landscape, under a range of meteorological conditions. Dogs were highly successful in locating the human target hidden 800 m from the start location (93% success). Humidity and air temperature had a significant effect on search strategy: as air conditions became cooler and more humid, dogs searched significantly closer to the experimental trail. Dogs also modified their speed and head position according to their search location distance from the experimental trail. When close to the trail, dogs searched with their head up and ran quickly but when their search took them farther from the trail, they were more likely to search with their nose to the ground, moving more slowly. This study of a mammalian species responding to localized shifts in ambient conditions lays the foundation for future studies of olfactory orientation, and the development of a highly tractable mammalian species for such research.

Jacobs LF (2019) The navigational nose: a new hypothesis for the function of the human external pyramid. J Exp Biol 222:jeb186924. https://doi.org/10.1242/jeb.186924

One of the outstanding questions in evolution is why Homo erectus became the first primate species to evolve the external pyramid, i.e. an external nose. The accepted hypothesis for this trait has been its role in respiration, to warm and humidify air as it is inspired. However, new studies testing the key assumptions of the conditioning hypothesis, such as the importance of turbulence to enhance heat and moisture exchange, have called this hypothesis into question. The human nose has two functions, however, respiration and olfaction. It is thus also possible that the external nose evolved in response to selection for olfaction. The genus Homo had many adaptations for long-distance locomotion, which allowed Homo erectus to greatly expand its species range, from Africa to Asia. Long-distance navigation in birds and other species is often accomplished by orientation to environmental odors. Such olfactory navigation, in turn, is enhanced by stereo olfaction, made possible by the separation of the olfactory sensors. By these principles, the human external nose could have evolved to separate olfactory inputs to enhance stereo olfaction. This could also explain why nose shape later became so variable: as humans became more sedentary in the Neolithic, a decreasing need for long-distance movements could have been replaced by selection for other olfactory functions, such as detecting disease, that would have been critical to survival in newly dense human settlements.

Delgado, M. M, and L. F Jacobs. How squirrels protect their caches: location,
conspicuousness during caching, and proximity to kin influence cache lifespan. BioRxiv 6
(August 16, 2019): 338–45. https://www.biorxiv.org/content/10.1101/738237v1

By genotyping a subpopulation of Berkeley squirrels, Mikel showed that that scatter hoarding fox squirrels placed caches closer to caches made by their close relatives. This suggests that foraging decisions are influenced by kin selection, as the loss of caches to pilfering relatives would be offset by inclusive fitness. Her study also identified key strategic choices squirrels make while caching and how this influences how long the cache remains hidden before it is retrieved or pilfered.

Delgado, M.M. & Jacobs, L.F., 2017. Caching for where and what: evidence for a mnemonic strategy in a scatter-hoarder. Royal Society Open Science, 4(9), pp.170958–6.

Squirrels organize their caches spatially by the species of nut. Such ‘spatial chunking’ increases the accuracy of memory recall in other species and probably reduces the cognitive load of building and managing an optimal cache map.

Delgado, M.M. and Jacobs, L.F. (2016). Inaccessibility of reinforcement increases persistence and signaling behavior in the fox squirrel, Sciurus niger. Journal of Comparative Psychology. 130(2): 128-137.

Is frustration adaptive? See the experiment here in this short film by KQED http://”Watch Those Frustrated Squirrels”

Jacobs, L. F., Arter, J., Cook, A., & Sulloway, F. J. (2015). Olfactory orientation and navigation in humans. PLoS ONE, 10(6), e0129387. http://doi.org/10.1371/journal.pone.0129387.s001

Although predicted by theory, there is no direct evidence that an animal can define an arbitrary location in space as a coordinate location on an odor grid. Here we show that humans can do so. Using a spatial match-to-sample procedure, humans were led to a random location within a room diffused with two odors. After brief sampling and spatial disorientation, they had to return to this location. Over three conditions, participants had access to different sensory stimuli: olfactory only, visual only, and a final control condition with no olfactory, visual, or auditory stimuli. Humans located the target with higher accuracy in the olfactiononly condition than in the control condition and showed higher accuracy than chance. Thus a mechanism long proposed for the homing pigeon, the ability to define a location on a map constructed from chemical stimuli, may also be a navigational mechanism used by humans.

Jacobs, L. F., & Menzel, R. (2014). Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab. Movement Ecology, 2(1), 1–22. http://doi.org/10.1186/2051-3933-2-3

Space is continuous. But the communities of researchers that study the cognitive map in non-humans are strangely divided, with debate over its existence found among behaviorists but not neuroscientists. To reconcile this and other debates within the field of navigation, we return to the concept of the parallel map theory, derived from data on hippocampal function in laboratory rodents. Here the cognitive map is redefined as the integrated map, which is a construction of dual mechanisms, one based on directional cues (bearing map) and the other on positional cues (sketch map). We propose that the dual navigational mechanisms of pigeons, the navigational map and the familiar area map, could be homologous to these mammalian parallel maps; this has implications for both research paradigms. Moreover, this has implications for the lab. To create a bearing map (and hence integrated map) from extended cues requires self-movement over a large enough space to sample and model these cues at a high resolution. Thus a navigator must be able to move freely to map extended cues; only then should the weighted hierarchy of available navigation mechanisms shift in favor of the integrated map. Because of the paucity of extended cues in the lab, the flexible solutions allowed by the integrated map should be rare, despite abundant neurophysiological evidence for the existence of the machinery needed to encode and map extended cues through voluntary movement. Not only do animals need to map extended cues but they must also have sufficient information processing capacity. This may require a specific ontogeny, in which the navigator’s nervous system is exposed to naturally complex spatial contingencies, a circumstance that occurs rarely, if ever, in the lab. For example, free-ranging, flying animals must process more extended cues than walking animals and for this reason alone, the integrated map strategy may be found more reliably in some species. By taking concepts from ethology and the parallel map theory, we propose a path to directly integrating the three great experimental paradigms of navigation: the honeybee, the homing pigeon and the laboratory rodent, towards the goal of a robust, unified theory of animal navigation.

Delgado, M. M., Nicholas, M., Petrie, D. J., & Jacobs, L. F. (2014). Fox squirrels match food assessment and cache effort to value and scarcity. PLoS ONE, 9(3), e92892. http://doi.org/10.1371/journal.pone.0092892.s003

Scatter hoarders must allocate time to assess items for caching, and to carry and bury each cache. Such decisions should be driven by economic variables, such as the value of the individual food items, the scarcity of these items, competition for food items and risk of pilferage by conspecifics. The fox squirrel, an obligate scatter-hoarder, assesses cacheable food items using two overt movements, head flicks and paw manipulations. These behaviors allow an examination of squirrel decision processes when storing food for winter survival. We measured wild squirrels’ time allocations and frequencies of assessment and investment behaviors during periods of food scarcity (summer) and abundance (fall), giving the squirrels a series of 15 items (alternating five hazelnuts and five peanuts). Assessment and investment per cache increased when resource value was higher (hazelnuts) or resources were scarcer (summer), but decreased as scarcity declined (end of sessions). This is the first study to show that assessment behaviors change in response to factors that indicate daily and seasonal resource abundance, and that these factors may interact in complex ways to affect food storing decisions. Food-storing tree squirrels may be a useful and important model species to understand the complex economic decisions made under natural conditions.

Evan L. MacLean, Brian A. Hare, Charles L. Nunn, Elsa Addessi, Federica Amici, Rindy C. Anderson, Filippo Aureli, Joseph M. Baker, Amanda E. Bania, Allison M. Barnard, Neeltje J. Boogert, Elizabeth M. Brannon, Emily E. Bray, Joel Bray, Lauren J. N. Brent, Judith M. Burkart, Josep Call, Jessica F. Cantlon, Lucy G. Cheke, Nicola S. Clayton, Mikel M. Delgado, Louis J. DiVincenti, Kazuo Fujita, Chihiro Hiramatsu, Lucia F. Jacobs, Kerry E. Jordan, Jennifer R. Laude, Kristin L. Leimgruber, Emily J. E. Messer, Antonio C. de A. Moura, Ljerka Ostojić, Alejandra Picard, Michael L. Platt, Joshua M. Plotnik, Friederike Range, Simon M. Reader, Rachna B. Reddy, Aaron A. Sandel, Laurie R. Santos, Katrin Schumann, Amanda M. Seed, Kendra B. Sewall, Rachael C. Shaw, Katie E Slocombe, Yanjie Su, Ayaka Takimoto, Jingzhi Tan, Ruoting Tao, Carel P. van Schaik, Zsófia Virányi, Elisabetta Visalberghi, Jordan C. Wade, Arii Watanabe, Jane Widness, Thomas R. Zentall, Yini Zhao. (2014) The evolution of self-control. Proceedings of the National Academy of Sciences, 111(20), E2140–8. doi:10.1073/pnas.1323533111.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Bettis TJ, Jacobs LF (2013) Sex differences in memory for landmark arrays in C57BL/J6 mice. Animal Cognition 16:873–882. https://doi.org/10.1007/s10071-013-0619-x

Cook, A., Arter, J., & Jacobs, L. F. (2013). My owner, right or wrong: the effect of familiarity on the domestic dog’s behavior in a food-choice task. Animal Cognition, 17(2), 461–470. http://doi.org/10.1007/s10071-013-0677-0

Waismeyer, A. S., & Jacobs, L. F. (2013). The emergence of flexible spatial strategies in young children. Developmental Psychology, 49(2), 232–242. http://doi.org/10.1037/a0028334

Jacobs, L. F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci, 109, 10693–10700. http://doi.org/10.1073/pnas.1201880109

Bettis, T., & Jacobs, L. F. (2012). Sex differences in object recognition are modulated by object similarity. Behavioural Brain Research, 233(2), 288–292. http://doi.org/10.1016/j.bbr.2012.04.028

Chai, X. J., & Jacobs, L. F. (2012). Digit ratio predicts sense of direction in women. PLoS ONE, 7(2), e32816. http://doi.org/10.1371/journal.pone.0032816

Kleschevnikov, A. M., Belichenko, P. V., Faizi, M., Jacobs, L. F., Htun, K., Shamloo, M., & Mobley, W. C. (2012). Deficits in cognition and synaptic plasticity in a mouse model of Down Syndrome ameliorated by GABAB receptor antagonists. Journal of Neuroscience, 32(27), 9217–9227. http://doi.org/10.1523/JNEUROSCI.1673-12.2012

MacLean, E.L., Matthews, L.J., Hare, B.A., Nunn, C.L., Anderson, R.C., Aureli, F., Brannon, E.M., Call, J., Drea, C.M., Emery, N.J., Haun, D.B., Herrmann, E., Jacobs, L.F., Platt, M.L., Rosati, A.G., Sandel, A.A., Schroepfer, K.K., Seed, A.M., Tan, J., van Schaik, C.P., and Wobber, V. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition 15, 223-238. https://doi.org/10.1007/s10071-011-0448-8.

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Wiener, J., Shettleworth, S., Bingman, V.P., Cheng, K., Healy, S., Jacobs, L.F., Jeffery, K.J., Mallot, H.A., Menzel, R., and Newcombe, N.S. (2011). Animal Navigation – A Synthesis. In Animal Thinking: Contemporary Issues in Comparative Cognition, R. Menzel, and J. Fischer, eds. (Cambridge, MA, MIT Press).

Waisman, A. S., Lucas, C. G., Griffiths, T. L., & Jacobs, L. F. (2011). A Bayesian model of navigation in squirrels. Presented at the Proc 33rd Annual Conf Cog Sci Society.

Chai, X. J., & Jacobs, L. F. (2010). Effects of cue types on sex differences in human spatial memory. Behavioural Brain Research, 208(2), 336–342. http://doi.org/10.1016/j.bbr.2009.11.039

Chai, X. J., Ofen, N., Jacobs, L. F., & Gabrieli, J. D. E. (2010). Scene complexity: influence on perception, memory, and development in the medial temporal lobe. Frontiers in Human Neuroscience, 4, 21–10. http://doi.org/10.3389/fnhum.2010.00021

Chai, X. J., & Jacobs, L. F. (2009). Sex differences in directional cue use in a virtual landscape. Behavioral Neuroscience, 123(2), 276–283. http://doi.org/10.1037/a0014722

Bettis, T. J., & Jacobs, L. F. (2009). Sex-specific strategies in spatial orientation in C57BL/6J mice. Behavioural Processes.

Preston SD, Jacobs LF (2009) Mechanisms of cache decision making in fox squirrels (Sciurus niger). J Mammal 90:787–795. https://doi.org/10.1644/08-mamm-a-254.1

The cache decisions of scatter-hoarding animals are influenced by a number of factors, including satiety, food quality, number of competitors, and the risk of predation and pilferage. However, it is unknown how animals assess these variables. We investigated this process experimentally in free-ranging fox squirrels (Sciurus niger) by measuring the effects of nut characteristics and social context on nut-handling behavior and subsequent cache decisions. We found that a behavior involved in nut handling, the head flick, was correlated with nut quality, shell presence, the decision to cache rather than eat the nut, and the time and energy spent caching. In contrast, a 2nd nut-handling behavior, the paw maneuver, was correlated with the social context but not the cache decision, and may instead reflect a response to social competition. Our results suggest that fox squirrels assess nut quality using overt, observable nut-handling behaviors. The experimental study of these behaviors can help us understand how animals use information about food and the social context to make adaptive food-storing decisions.

Jacobs, L. F. (2009). The role of social selection in the evolution of hippocampal specialization. In L. Tommasi, M. A. Peterson, & L. Nadel (Eds.), Cognitive Biology: Evolutionary and Developmental Perspectives on Mind. Cambridge, MA: MIT Press.

Waisman AS, Jacobs LF (2008) Flexibility of cue use in the fox squirrel (Sciurus niger). Anim Cogn 11:625–636. https://doi.org/10.1007/s10071-008-0152-5

Recent work on captive flying squirrels has demonstrated a novel degree of flexibility in the use of different orientation cues. In the present study, we examine to what extent this flexibility is present in a free-ranging population of another tree squirrel species, the fox squirrel. We trained squirrels to a rewarded location within a square array of four feeders and then tested them on transformations of the array that either pitted two cue types against one cue type, the majority tests, or all cue types against each other, the forced-hierarchy test. In Experiment 1, squirrels reoriented to the two-cue-type location in all majority tests and to the location indicated by the visual features of the feeders in the forced-hierarchy test. This preference for visual features runs contrary to previous studies that report the use of spatial cues over visual features in food-storing species. In Experiments 2–5 we tested squirrels with different trial orders (Experiments 2 and 3), a different apparatus (Experiment 4) and at different times of the year (Experiment 5) to determine why these squirrels had chosen to orient using visual features in the first experiment. Like captive flying squirrels, free-ranging fox squirrels showed a large degree of flexibility in their use of cues. Furthermore, their cue use appeared to be sensitive both to changes in the test apparatus and the season in which we tested. Altogether our results suggest that the study of free-ranging animals over a variety of conditions is necessary for understanding spatial cognition.

Barkley, C., & Jacobs, L. F. (2007). Sex and species differences in spatial memory in food-storing kangaroo rats. Animal Behaviour, 73(2), 321–329. http://doi.org/10.1016/j.anbehav.2006.07.009

Scatter-hoarding birds show superior performance in many spatial memory tasks and appear to relocate sites using different cues than nonscatter hoarders. However, there have not been similar studies of cue use and memory for locations by mammals that differ in their reliance on scatter hoards for survival. Here we report differences in spatial memory in two species of kangaroo rats that are predicted by foraging ecology. Merriam’s kangaroo rat, Dipodomys merriami, a scatter hoarder that hoards intensively, showed accurate memory on a cache simulation task, which required the rat to find four predetermined locations after a 24-h delay. In contrast, the leaf-eating specialist Great Basin kangaroo rat, D. microps, which relies less on scatter hoarding, showed poorer accuracy under the same experimental conditions. The presence of local landmarks did not differentially affect recovery in the two species of kangaroo rats, unlike previous studies in birds. We did find a significant interaction between the presence of local landmarks and sex on target recovery. Female performance was significantly impaired by the absence of local landmarks, while male performance was unaltered. Spatial ecology predicted both species and sex differences in spatial memory in kangaroo rats.

Gibbs SEB, Lea SEG, Jacobs LF (2007) Flexible use of spatial cues in the southern flying squirrel (Glaucomys volans). Anim Cogn 10:203–209. https://doi.org/10.1007/s10071-006-0059-y

Insects, birds, and mammals have been shown capable of encoding spatial information in memory using multiple strategies or frames of reference simultaneously. These strategies include orientation to a goal-specific cue or beacon, to the position of the goal in an array of local landmarks, or to its position in the array of distant landmarks, also known as the global frame of reference. From previous experiments, it appears that birds and mammals that scatter hoard rely primarily on a global frame of reference, but this generalization depends on evidence from only a few species. Here we examined spatial memory in a previously unstudied scatter hoarder, the southern flying squirrel. We dissociated the relative weighting of three potential spatial strategies (beacon, global, or relative array strategy) with three probe tests: transposition of beacon and the rotation or the expansion of the array. The squirrels’ choices were consistent with a spatial averaging strategy, where they chose the location dictated by at least two of the three strategies, rather than using a single preferred frame of reference. This adaptive and flexible heuristic has not been previously described in animal orientation studies, yet it may be a common solution to the universal problem of encoding and recalling spatial locations in an ephemeral physical landscape.

Adams-Hunt, Melissa M., and Jacobs, Lucia F. (2007). Learning to forage. In: Foraging: Behavior and Ecology, D.W. Stephens, J.S. Brown, and R.C. Ydenberg, eds. (Chicago, IL, University of Chicago), p. 576.

Jacobs, L. F. (2006). From movement to transitivity: the role of hippocampal parallel maps in configural learning. Reviews in the Neurosciences, 17(1-2), 99–109.

Whether spatial learning is a special case of configural or relational learning, or whether abstract principles evolved from the concrete need to navigate in space, is a question of long-standing debate. The parallel map theory of hippocampal function offers a resolution of the debate by redefining ‘spatial learning’ as two parallel, geometric processes, Euclidean metric and topological. Moreover, these processes are subserved by independent hippocampal subfields that underlie two ways of representing space, the bearing and the sketch map. It is possible that configural and relational learning, like spatial learning, should also be distinguished in this way. Transitive inference, requiring the construction of a value gradient, could be analyzed as a Euclidean metric problem. In contrast, transverse patterning could be seen as a topological analysis of the relationships among discrete objects. If this interpretation is correct, lesions to the primary bearing map structure (dentate gyrus) should impair transitivity while lesions to the primary sketch map structure (CA1) should impair transverse patterning and similar topological tasks. Recent results from diverse species and tasks lend support to these predictions, suggesting that the hippocampus not only creates parallel maps but uses these maps to solve more abstract configural or relational problems.

Hermes, G. L., Jacobs, L. F., & McClintock, M. (2005). The sectored foraging field: A novel design to quantify spatial strategies, learning, memory, and emotion. Neurobiology of Learning and Memory, 84(1), 69–73.

Preston SD, Jacobs LF (2005) Cache decision making: The effects of competition on cache decisions in Merriam’s Kangaroo Rat (Dipodomys merriami). J Comp Psychol 119:187–196. https://doi.org/10.1037/0735-7036.119.2.187

Caching food is an economic, decision-making process that requires animals to take many factors into account, including the risk of pilferage. However, little is known about how food-storing animals determine the risk of pilferage. In this study, the authors examined the effect of a dominant competitor species on the caching and behavior of Merriam’s kangaroo rat (Dipodomys merriami). The authors found that, as with conspecific competitors, kangaroo rats did not alter caching in response to the mere presence of a heterospecific competitor, but moved caches to an unpreferred area when the competitor’s presence was paired with pilferage. These data suggest that Merriam’s kangaroo rat assesses pilfer risk from actual pilferage by a competitor and adaptively alters cache strategy to minimize future risk.

Jacobs, L. F., & Schenk, F. (2003). Unpacking the cognitive map: the parallel map theory of hippocampal function. Psychological Review, 110(2), 285–315.

In the parallel map theory, the hippocampus encodes space with 2 mapping systems. The bearing map is constructed primarily in the dentate gyrus from directional cues such as stimulus gradients. The sketch map is constructed within the hippocampus proper from positional cues. The integrated map emerges when data from the bearing and sketch maps are combined. Because the component maps work in parallel, the impairment of one can reveal residual learning by the other. Such parallel function may explain paradoxes of spatial learning, such as learning after partial hippocampal lesions, taxonomic and sex differences in spatial learning, and the function of hippocampal neurogenesis. By integrating evidence from physiology to phylogeny, the parallel map theory offers a unified explanation for hippocampal function.

Jacobs, L. F. (2003). The evolution of the cognitive map. Brain, Behavior and Evolution, 62(2), 128–139. http://doi.org/10.1159/000072443

The hippocampal formation of mammals and birds mediates spatial orientation behaviors consistent with a map-like representation, which allows the navigator to construct a new route across unfamiliar terrain. This cognitive map thus appears to underlie long-distance navigation. Its mediation by the hippocampal formation and its presence in birds and mammals suggests that at least one function of the ancestral medial pallium was spatial navigation. Recent studies of the goldfish and certain reptile species have shown that the medial pallium homologue in these species can also play an important role in spatial orientation. It is not yet clear, however, whether one type of cognitive map is found in these groups or indeed in all vertebrates. To answer this question, we need a more precise definition of the map. The recently proposed parallel map theory of hippocampal function provides a new perspective on this question, by unpacking the mammalian cognitive map into two dissociable mapping processes, mediated by different hippocampal subfields. If the cognitive map of non-mammals is constructed in a similar manner, the parallel map theory may facilitate the analysis of homologies, both in behavior and in the function of medial pallium subareas.

Preston, S. D., & Jacobs, L. F. (2001). Conspecific pilferage but not presence affects Merriam’s kangaroo rat cache strategy. Behavioral Ecology, 12(5), 517–523.

We investigated the effects of pilferage on caching behavior in the Merriam’s kangaroo rat by manipulating two factors associated with pilferage: the presence of a conspecific, and the opportunity for pilferage. In one experiment we assessed animals in either ‘‘Stealer’’ or ‘‘Victim’’ roles and measured changes in caching, space use, and behavior after caches were pilfered. Victims shifted from a majority scatter-hoarding to a majority larder-hoarding strategy after their caches were pilfered by the Stealer. In Experiment 2, we measured changes after exposure to a conspecific when there was no pilferage, with or without prior exposure to pilferage from Experiment 1. Merriam’s kangaroo rats were vigilant when a conspecific was present, but did not change cache strategy. Prior exposure did not have any major effect on caching or behavior. Food storage is an economic decision that is often made by a solitary forager. Our results suggest that social competition nonetheless influences such economic decisions, even in a nonsocial forager.

Jacobs, L.F. (2000). Sexual differentiation and cognitive function. In: Gender and Society: the 1995 Herbert Spencer Lectures, S. Iversen, ed. (Oxford, UK, Oxford University Press).

Lavenex, P., Steele, M. A., & Jacobs, L. F. (2000). Sex differences, but no seasonal variations in the hippocampus of food‐caching squirrels: A stereological study. Journal of Comparative Neurology, 425(1), 152–166.

Lavenex, P., Steele, M. A., & Jacobs, L. F. (2000). The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. European Journal of Neuroscience, 12(2), 643–648.

Jacobs, L. F., & Shiflett, M. W. (1999). Spatial orientation on a vertical maze in free-ranging fox squirrels ( Sciurus niger). Journal of Comparative Psychology, 113(2), 116–127.

To determine how squirrels return to remembered locations in an arboreal environment, wild fox squirrels (Sciurus niger) were trained on an outdoor vertical maze. Squirrels were trained on 1 route and tested with all routes accessible. Possible mechanisms of spatial orientation were distinguished with manipulations such as rotations, shifts, and blocked routes. Squirrels consistently used an extra-maze, allothetic frame of reference to orient and appeared to organize their memory of the route hierarchically. This study demonstrates that a laboratory technique, the maze, can be successfully brought into the field to measure mechanisms of spatial orientation under natural conditions in free-ranging wild rodents. Such studies will allow researchers to determine what kind of spatial information is acquired by wild animals under natural conditions and how this information is used.

Barkley, C., & Jacobs, L. F. (1998). Visual environment and delay affect cache retrieval accuracy in a food-storing rodent. Learning & Behavior, 26(4), 439–447.

Many scatter-hoarding species use spatial memory to relocate their food caches. Two factors can affect spatial memory: the availability of landmarks in the environment, and the latency between learning and recall. Using a 2 × 2 factorial design, we determined the effect of these factors on cache retrieval accuracy in Merriam’s kangaroo rats (Dipodomys merriami). Kangaroo rats cached seeds in an arena under conditions that varied by retrieval interval (1 or 10 days) and by number of landmarks (0 or 16 landmarks). After 1 day, they recovered equal proportions of caches in both landmark conditions. After 10 days, they recovered more caches in the 16-landmark condition than in the bare condition. This is the first study to show that landmarks are necessary for accurate cache recovery after long delays. This result is consistent with maze studies that have shown that landmarks reduce proactive interference and that delay increases proactive interference.

Lavenex, P., Shiflett, M. W., Lee, R. K., & Jacobs, L. F. (1998). Spatial versus nonspatial relational learning in free-ranging fox squirrels (Sciurus niger). Journal of Comparative Psychology, 112(2), 127–136.

Feener, D. H., Jacobs, L. F., & Schmidt, J. O. (1996). Specialized parasitoid attracted to a pheromone of ants. Animal Behaviour, 51(1), 61–66.

Jacobs, L. F. (1996). Sexual selection and the brain. Trends Ecol Evol, 11(2), 82–86.

Sex differences are intrinsically interesting, particularly in the brain. When sexually dimorphic structures mediate learning, and when such learning ability is necessary to compete for mates, then such differences are best understood within the framework of sexual selection. By categorizing recent studies of sex differences in the brain by their role in mate competition, theories of sexual selection can be used to predict and characterize the occurrence of dimorphisms among species with different mating systems.

Jacobs, L. F. (1996). The economy of winter: phenotypic plasticity in behavior and brain structure. The Biological Bulletin, 191(1), 92–100. https://doi.org/10.2307/1543068

Mobile animals must learn the spatial distributions of resources. The cost of foraging increases dramatically for temperate-zone animals during the winter. Two strategies may be used to balance the energetic budget: reducing costs of foraging and reducing need to forage. Both strategies are correlated with changes in brain structure, specifically in the hippocampus, a fore-brain structure used by birds and mammals to map spatial distributions of resources. Small mammals that reduce their need to forage, through hibernation or reduction in body size, show a specific reduction in the structure and size of the hippocampus. The costs of foraging can be also decreased by migration to better foraging conditions or by food-storing, both of which decrease the temporal heterogeneity of food resources. Both of these latter strategies are associated with increased hippocampal structure; for food-storing birds, this increase is a seasonal phenomenon. Thus not only behavior, but also learning ability and even brain structures in adult animals, may be phenotypically plastic in response to the changing demands of the environment.

Jacobs, L. F. (1995). The ecology of spatial cognition: adaptive patterns of hippocampal size and space use in wild rodents. In E. Alleva, A. Fasolo, H.-P. Lipp, & L. Nadel (Eds.), (pp. 301–322). Dordrecht: Behavioural Brain Research in Naturalistic and Semi-Naturalistic Setting.

Jacobs, L. F., & Spencer, W. D. (1994). Natural space-use patterns and hippocampal size in kangaroo rats. Brain, Behavior and Evolution, 44(3), 125–132.

The size of the hippocampus, a forebrain structure that processes spatial information, correlates with the need to relocate food caches by passerine birds and with sex-specific patterns of space use in microtine rodents. The influences on hippocampal anatomy of sexual selection within species, and natural selection between species, have not yet been studied in concert, however. Here we report that natural space-use patterns predict hippocampal size within and between two species of kangaroo rats (Dipodomys). Differences in foraging behavior suggest that Merriam”s kangaroo rats (D. merriami) require better spatial abilities than bannertail kangaroo rats (D. spectabilis). Sex-specific differences in mating strategy suggest that males of both species require more spatial ability than females. As predicted, hippocampal size (relative to brain size) is larger in Merriam”s than in bannertail kangaroo rats, and males have larger hippocampi than females in both species. Males of a third species (D. ordii) also have smaller hippocampi than Merriam’s kangaroo rat males, despite being similar to Merriam”s in brain and body size. These results suggest that both natural and sexual selection affect the relative size and perhaps function of mammalian hippocampi. They also reassert that measures of functional subunits of the brain reveal more about brain evolution than measures of total brain size.

Daly, M., Behrends, P., Wilson, M. I., & Jacobs, L. F. (1992). Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Animal Behaviour, 44(1), 1–9.

Collaboration with Margo Wilson and Martin Daly

Daly M, Jacobs LF, Wilson MI, Behrends PR (1992) Scatter hoarding by kangaroo rats (Dipodomys merriami) and pilferage from their caches. Behav Ecol 3:102–111. https://doi.org/10.1093/beheco/3.2.102

Collaboration with Margo Wilson and Martin Daly

We observed radio-implanted Merriam’s kangaroo rats disposing of 10-g bonanzas of rolled oats in 48 trials in the field. The principal determinant of the initial disposition of discovered food was apparently its distance from the day burrow: food found within about 10m was mainly larder hoarded, whereas food encountered farther afield was usually dispersed immediately in shallow caches. Cache sites were newly dug for the purpose and not reused; most caches were nearer the current day burrow than was the food source, but a few were placed far from both the cacher’s day burrow and its habitual nocturnal range. An experiment with artificial caches indicated that security from discovery increases with spacing and with proximity to perennial shrubs. Nine kangaroo rats cached dyed food, and fecal dye traces revealed extensive pilferage from five of them, by both conspecifics and other rodent species. Limited evidence indicates that food encountered nearer home and initially larder hoarded was more secure from pilferage than food initially scattered, and yet kangaroo rats were observed to scatter caches soon after initial larder hoarding. A kangaroo rat whose dyed stores escaped pilferage fed from them at intervals for at least 12 days. Even cachers who incurred pilferage made as much, or more, use of their caches as any thief, suggesting that scattering caches may be a defense against catastrophic losses.

Daly, M., Wilson, M. I., Behrends, P., & Jacobs, L. F. (1992). Sexually differentiated effects of radio transmitters on predation risk and behaviour in kangaroo rats (Dipodomys merriami). Canadian Journal of Zoology, 70(9), 1851–1855.

Jacobs LF (1992) Memory for cache locations in Merriam’s kangaroo rats. Animal Behaviour 43:585–593. https://doi.org/10.1016/0003-3472(92)90081-j

The ability of Merriam’s kangaroo rats, Dipodono’s merriami, to remember the location of food caches and to relocate caches in the absence of the odour of buried seeds was examined. Eight wild-caught kangaroo rats cached seeds in an experimental arena, and retrieved them 24 h later. Before retrieval, all odours associated with the cache sites were removed and seeds were replaced in only halfofthe cache sites. During retrieval, kangaroo rats were significantly more likely to search cache sites, with or without seeds, than non-cache sites. Non-cache sites were primarily investigated after all cache sites had been searched, indicating that search of non-cache sites did not denote an error in cache retrieval. These results suggest that kangaroo rats can remember the locations of food caches, and can relocate cache sites even when there is no odour of buried seeds. To estimate the advantage enjoyed by the forager with greater information, a second experiment compared an owner’s success in retrieving its caches with the success of naive kangaroo rats searching for these same caches. Nine wild-caught kangaroo rats were allowed to search for caches that were distributed in the same spatial pattern as that created by one kangaroo rat from the first experiment. The naive subjects found significantly fewer caches than had the cache owner in the same length of time. This suggests that the use of spatial memory by a Merriam’s kangaroo rat to relocate its food caches gives it a competitive advantage over other kangaroo rats that may be searching for its caches.

Jacobs LF (1992) The effect of handling time on the decision to cache by grey squirrels. Anim Behav 43:522–524. https://doi.org/10.1016/s0003-3472(05)80111-3

Sherry DF, Jacobs LF, Gaulin SJC (1992) Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298–303. https://doi.org/10.1016/0166-2236(92)90080-r

The hippocampus plays an important role in spatial memory and spatial cognition in birds and mammals. Natural selection, sexual selection and artificial selection have resulted in an increase in the size of the hippocampus in a remarkably diverse group of animals that rely on spatial abilities to solve ecologically important problems. Food-storing birds remember the locations of large numbers of scattered caches. Polygynous male voles traverse large home ranges in search of mates. Kangaroo rats both cache food and exhibit a sex difference in home range size. In all of these species, an increase in the size of the hippocampus is associated with superior spatial ability. Artificial selection for homing ability has produced a comparable increase in the size of the hippocampus in homing pigeons, compared with other strains of domestic pigeon. Despite differences among these animals in their histories of selection and the genetic backgrounds on which selection has acted, there is a common relationship between relative hippocampal size and spatial ability.

Jacobs LF, Liman Emily R. (1991) Grey squirrels remember the locations of buried nuts. Anim Behav 41:103–110. https://doi.org/10.1016/s0003-3472(05)80506-8

It has previously been assumed that grey squirrels, Sciurus carolinensis, cannot remember the locations of nuts they have buried, and hence must relocate nuts by their odour. This assumption was tested by measuring the accuracy of cache retrieval of captive squirrels. Each squirrel was released alone into an outdoor arena, where it cached 10 hazelnuts. After a delay of 2,4 or 12 days, each squirrel was returned to the arena and tested for its ability to retreve nuts from its own cache sites and from 10 cache sites used by other squirrels. Although each squirrel’s own caches were close to the caches of other squirrels, the squirrels retrieved significantly more nuts from their own sites than from sites used by other squirrels, after all delays. The retrieval accuracy of the squirrels under these conditions indicates that while grey squirrels can locate buried nuts by their odour, they can also remember the individual locations of nuts they have buried.

Jacobs LF, Gaulin SJ, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc National Acad Sci 87:6349–6352. https://doi.org/10.1073/pnas.87.16.6349

In a study of two congeneric rodent species, sex differences in hippocampal size were predicted by sex-specific patterns of spatial cognition. Hippocampal size is known to correlate positively with maze performance in laboratory mouse strains and with selective pressure for spatial memory among passerine bird species. In polygamous vole species (Rodentia: Microtus), males range more widely than females in the field and perform better on laboratory measures of spatial ability; both of these differences are absent in monogamous vole species. Ten females and males were taken from natural populations of two vole species, the polygamous meadow vole, M. pennsylvanicus, and the monogamous pine vole, M. pinetorum. Only in the polygamous species do males have larger hippocampi relative to the entire brain than do females. Two-way analysis of variance shows that the ratio of hippocampal volume to brain volume is differently related to sex in these two species. To our knowledge, no previous studies of hippocampal size have linked both evolutionary and psychometric data to hippocampal dimensions. Our controlled comparison suggests that evolution can produce adaptive sex differences in behavior and its neural substrate.

Daly M, Wilson M, Behrends PR, Jacobs LF (1990) Characteristics of kangaroo rats, Dipodomys merriami, associated with differential predation risk. Anim Behav 40:380–389. https://doi.org/10.1016/s0003-3472(05)80934-0.

Between 1980 and 1990, 176 adult Merriam’s kangaroo rats were subcutaneously implanted with radio transmitters and tracked for a total of 6316 animal-days at a California site, prior to and during reproductive seasons. Thirty-six animals are known to have been killed by predators, and 14 who disappeared abruptly are also presumed victims. These 50 cases permit various analyses of differential predation risk. Males incurred a predation rate (4·22 deaths per animal-year) more than twice that of females (2·01); this sex difference in mortality was apparently absent or reversed after the breeding season. Both male and female victims travelled significantly greater distances between successive radio-locations shortly before their deaths than surviving same-sex animals tracked contemporaneously. Rather than being selective for the feeble, predation on kangaroo rats is selective for the mobile.

Sengelaub, D. R., Jacobs, L. F., & Finlay, B. L. (1985). Regional differences in normally occurring cell death in the developing hamster lateral geniculate nuclei. Neuroscience Letters, 55(2), 103–108.