Variation in hippocampal morphology along an environmental gradient: controlling for the effects of day length

Environmental conditions may create increased demands for memory, which in turn may affect specific brain regions responsible for memory function. This may occur either via phenotypic plasticity or selection for individuals with enhanced cognitive abilities. For food-caching animals, in particular, spatial memory appears to be important because it may have a direct effect on fitness via their ability to accurately retrieve food caches. Our previous studies have shown that caching animals living in more harsh environments (characterized by low temperatures, high snow cover and short day lengths) possess more neurons within a larger hippocampus (Hp), a part of the brain involved in spatial memory. However, the relative role of each of these environmental features in the relationship is unknown. Here, we dissociate the effects of one theoretically important factor (day length) within the environmental severity/Hp relationship by examining food-caching birds (black-capped chickadee, Poecile atricapillus) selected at locations along the same latitude, but with very different climatic regimes. There was a significant difference in Hp attributes among populations along the same latitude with very different climatic features. Birds from the climatically mild location had significantly smaller Hp volumes and fewer Hp neurons than birds from the more harsh populations, even though all populations experienced similar day lengths. These results suggest that variables such as temperature and snow cover seem to be important even without the compounding effect of reduced day length at higher latitudes and suggest that low temperature and snow cover alone may be sufficient to generate high demands for memory and the hippocampus. Our data further confirmed that the association between harsh environment and the hippocampus in food-caching animals is robust across a large geographical area and across years.     

The effect of environmental harshness on neurogenesis: a large-scale comparison

Harsh environmental conditions may produce strong selection pressure on traits, such as memory, that may enhance fitness. Enhanced memory may be crucial for survival in animals that use memory to find food and, thus, particularly important in environments where food sources may be unpredictable. For example, animals that cache and later retrieve their food may exhibit enhanced spatial memory in harsh environments compared with those in mild environments. One way that selection may enhance memory is via the hippocampus, a brain region involved in spatial memory. In a previous study, we established a positive relationship between environmental severity and hippocampal morphology in food-caching black-capped chickadees (Poecile atricapillus). Here, we expanded upon this previous work to investigate the relationship between environmental harshness and neurogenesis, a process that may support hippocampal cytoarchitecture. We report a significant and positive relationship between the degree of environmental harshness across several populations over a large geographic area and (1) the total number of immature hippocampal neurons, (2) the number of immature neurons relative to the hippocampal volume, and (3) the number of immature neurons relative to the total number of hippocampal neurons. Our results suggest that hippocampal neurogenesis may play an important role in environments where increased reliance on memory for cache recovery is critical.     

Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli)

Earlier reports suggested that seasonal variation in food-caching behavior (caching intensity and cache retrieval accuracy) might correlate with morphological changes in the hippocampal formation, a brain structure thought to play a role in remembering cache locations. We demonstrated that changes in cache retrieval accuracy can also be triggered by experimental variation in food supply: captive mountain chickadees (Poecile gambeli) maintained on limited and unpredictable food supply were more accurate at recovering their caches and performed better on spatial memory tests than birds maintained on ad libitum food. In this study, we investigated whether these two treatment groups also differed in the volume and neuron number of the hippocampal formation. If variation in memory for food caches correlates with hippocampal size, then our birds with enhanced cache recovery and spatial memory performance should have larger hippocampal volumes and total neuron numbers. Contrary to this prediction we found no significant differences in volume or total neuron number of the hippocampal formation between the two treatment groups. Our results therefore indicate that changes in food-caching behavior and spatial memory performance, as mediated by experimental variations in food supply, are not necessarily accompanied by morphological changes in volume or neuron number of the hippocampal formation in fully developed, experienced food-caching birds.     

Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory

It is widely assumed that chronic stress and corresponding chronic elevations of glucocorticoid levels have deleterious effects on animals' brain functions such as learning and memory. Some animals, however, appear to maintain moderately elevated levels of glucocorticoids over long periods of time under natural energetically demanding conditions, and it is not clear whether such chronic but moderate elevations may be adaptive. I implanted wild-caught food-caching mountain chickadees (Poecile gambeli), which rely at least in part on spatial memory to find their caches, with 90-day continuous time-release corticosterone pellets designed to approximately double the baseline corticosterone levels. Corticosterone-implanted birds cached and consumed significantly more food and showed more efficient cache recovery and superior spatial memory performance compared with placebo-implanted birds. Thus, contrary to prevailing assumptions, long-term moderate elevations of corticosterone appear to enhance spatial memory in food-caching mountain chickadees. These results suggest that moderate chronic elevation of corticosterone may serve as an adaptation to unpredictable environments by facilitating feeding and food-caching behaviour and by improving cache-retrieval efficiency in food-caching birds.     

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.     

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli)

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.     

Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli)

Environmental perturbations increase adrenal activity in several vertebrates. Increases in corticosterone may serve as a proximate trigger whereby organisms can rapidly adapt their behavior to survive environmental fluctuations. In food-caching songbirds, inclement weather may present the need to alter caching and/or retrieval behaviors to ensure food supplies. We hypothesized that corticosterone may increase the rate of caching and/or retrieval behaviors in the mountain chickadee, a food-storing songbird, and tested if these potential effects were mediated by alterations in appetite, activity, or memory for cache sites. Corticosterone or vehicle was administered to subjects 5 min prior to either caching or recovery in a naturalistic laboratory paradigm during which we recorded the number of caching events, sites visited, and seeds eaten (caching) or caches recovered, total sites visited, cache-related visits, and non-cache-related visits (recovery). Data were analyzed using nested ANOVA for treatment within sequential trial. There was no effect on any caching behaviors following treatment. However, birds treated with corticosterone during retrieval recovered more seeds and tended to visit more cache-related sites than did controls. Since groups did not differ in the number of seeds eaten or the total number of sites visited, it seems unlikely that corticosterone affected appetite or activity. Rapid surges in corticosterone may increase the efficacy of an underlying memory process for cache sites which is reflected in higher cache recovery in corticosterone-treated birds than in controls. Thus, rapid alterations in plasma corticosterone following environmental change may alter memory-reliant behaviors which promote survival in the food-caching mountain chickadee.     

The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli)

It has been hypothesized that in avian social groups subordinate individuals should maintain more energy reserves than dominants, as an insurance against increased perceived risk of starvation. Subordinates might also have elevated baseline corticosterone levels because corticosterone is known to facilitate fattening in birds. Recent experiments showed that moderately elevated corticosterone levels resulting from unpredictable food supply are correlated with enhanced cache retrieval efficiency and more accurate performance on a spatial memory task. Given the correlation between corticosterone and memory, a further prediction is that subordinates might be more efficient at cache retrieval and show more accurate performance on spatial memory tasks. We tested these predictions in dominant-subordinate pairs of mountain chickadees (Poecile gambeli). Each pair was housed in the same cage but caching behavior was tested individually in an adjacent aviary to avoid the confounding effects of small spaces in which birds could unnaturally and directly influence each other's behavior. In sharp contrast to our hypothesis, we found that subordinate chickadees cached less food, showed less efficient cache retrieval, and performed significantly worse on the spatial memory task than dominants. Although the behavioral differences could have resulted from social stress of subordination, and dominant birds reached significantly higher levels of corticosterone during their response to acute stress compared to subordinates, there were no significant differences between dominants and subordinates in baseline levels or in the pattern of adrenocortical stress response. We find no evidence, therefore, to support the hypothesis that subordinate mountain chickadees maintain elevated baseline corticosterone levels whereas lower caching rates and inferior cache retrieval efficiency might contribute to reduced survival of subordinates commonly found in food-caching parids.     

Variation in hippocampal glial cell numbers in food‐caching birds from different climates

Enhancements to memory are associated with enhanced neural structures that support those capabilities. A great deal of work has examined this relationship in the context of natural variation in spatial memory capability and hippocampal (Hp) structure. Most studies have focused on volumetric and neuron measures, but have seldom examined the role of glial cells. Once considered involved only in supportive functions associated with neurons, the importance of glial cells in cognitive processes, including memory, is gaining more attention. Building upon our previous study on the relationship between the brain, memory, and environmental severity in food‐caching birds, we compared the total number of Hp glial cells in wild‐sampled and in lab‐reared (common garden) black‐capped chickadees (Poecile atricapillus) originating from two different environmental extremes. We found that birds from more harsh climate tended to have significantly more Hp glial cells than those from more mild climate and that lab‐reared chickadees had significantly fewer Hp glial cells compared to the wild‐sampled birds. These results suggest that population differences in glial numbers may be controlled, at least in part, by heritable mechanisms, but glial numbers appear to be additionally regulated by an individual's environment. The pattern of Hp glial cell abundance among our treatment groups closely followed that of the Hp volume, suggesting that Hp glial cell number may be associated with the Hp volume. Unlike Hp neurons, however, the number of Hp glial cells may be, at least in part, affected by an individual's experiences and environment. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 73: 480–485, 2013     

Sex,estradiol, and spatial memory in a food-caching corvid

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.     

Variation in memory and the hippocampus across populations from different climates: a common garden approach

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individual's experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captive-raised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.     

Population genetic structure and its implications for adaptive variation in memory and the hippocampus on a continental scale in food-caching black-capped chickadees

Food-caching birds rely on stored food to survive the winter, and spatial memory has been shown to be critical in successful cache recovery. Both spatial memory and the hippocampus, an area of the brain involved in spatial memory, exhibit significant geographic variation linked to climate-based environmental harshness and the potential reliance on food caches for survival. Such geographic variation has been suggested to have a heritable basis associated with differential selection. Here, we ask whether population genetic differentiation and potential isolation among multiple populations of food-caching black-capped chickadees is associated with differences in memory and hippocampal morphology by exploring population genetic structure within and among groups of populations that are divergent to different degrees in hippocampal morphology. Using mitochondrial DNA and 583 AFLP loci, we found that population divergence in hippocampal morphology is not significantly associated with neutral genetic divergence or geographic distance, but instead is significantly associated with differences in winter climate. These results are consistent with variation in a history of natural selection on memory and hippocampal morphology that creates and maintains differences in these traits regardless of population genetic structure and likely associated gene flow.     

Where's my dinner? Adult neurogenesis in free‐living food‐storing rodents

Postnatal hippocampal neurogenesis in wild mammals may play an essential role in spatial memory. We compared two species that differ in their reliance on memory to locate stored food. Yellow-pine chipmunks use a single cache to store winter food; eastern gray squirrels use multiple storage sites. Gray squirrels had three times the density of proliferating cells in the dentate gyrus (determined by Ki-67 immunostaining) than that found in chipmunks, but similar density of young neurons (determined by doublecortin immunostaining). Three explanations may account for these results. First, the larger population of young cells in squirrels may increase the flexibility of the spatial memory system by providing a larger pool of cells from which new neurons can be recruited. Second, squirrels may have a more rapid cell turnover rate. Third, many young cells in the squirrels may mature into glia rather than neurons. The densities of young neurons were higher in juveniles than in adults of both species. The relationship between adult age and cell density was more complex than that has been found in captive populations. In adult squirrels, the density of proliferating cells decreased exponentially with age, whereas in adult chipmunks the density of young neurons decreased exponentially with age.     

Mechanisms of Cache Retrieval in the Group Nesting Southern Flying Squirrel (Glaucomys volans)

We examined the proximate mechanisms of cache retrieval in the group‐living, southern flying squirrel, Glaucomys volans, through a series of behavioral experiments conducted in a large indoor arena. The effectiveness of several retrieval mechanisms was determined including spatial memory, olfaction, random searching and a heuristic under different environmental conditions. Our goal was to elucidate the hoarding strategy of individuals in a nest group and to address whether food storing individuals possess a retrieval advantage over pilfering nestmates. A storer's retrieval advantage is necessary for scatter hoarding to be an evolutionarily stable strategy (ESS) within aggregations of unrelated individuals. Our previous work has shown that, G. volans lives in such groups, and consequently it was important to address the storer's retrieval advantage under a range of environmental conditions. Initially in our baseline experiment, we developed methods to eliminate olfactory‐based retrieval and to control for random searching. Subsequently, we experimentally determined the effectiveness of cache retrieval via spatial memory, a heuristic and olfaction. We examined the mechanisms of cache retrieval in three additional experiments using two independent subject populations and found that under dry, odorless conditions spatial memory was the most effective retrieval mechanism in support of a storer's retrieval advantage. In a fifth experiment we examined cache retrieval under wet environmental conditions and showed that olfactory‐based retrieval was effective and the storer's advantage was reduced. We interpret these laboratory results based on considerations of natural environmental conditions and game theory. We propose a conditional ESS strategy where animals store and retrieve their own caches as the primary food hoarding tactic and opportunistically pilfer caches as a secondary tactic.     

Elements of episodic-like memory in animals

A number of psychologists have suggested that episodic memory is a uniquely human phenomenon and, until recently, there was little evidence that animals could recall a unique past experience and respond appropriately. Experiments on food-caching memory in scrub jays question this assumption. On the basis of a single caching episode, scrub jays can remember when and where they cached a variety of foods that differ in the rate at which they degrade, in a way that is inexplicable by relative familiarity. They can update their memory of the contents of a cache depending on whether or not they have emptied the cache site, and can also remember where another bird has hidden caches, suggesting that they encode rich representations of the caching event. They make temporal generalizations about when perishable items should degrade and also remember the relative time since caching when the same food is cached in distinct sites at different times. These results show that jays form integrated memories for the location, content and time of caching. This memory capability fulfils Tulving's behavioural criteria for episodic memory and is thus termed 'episodic-like'. We suggest that several features of episodic memory may not be unique to humans.     

Memory and Brain in Food‐Storing Birds: Space Oddities or Adaptive Specializations?

Scatterhoarding birds that cache food items have become an important model system for the study of spatial memory and its correlates in the brain. In particular, it has been suggested that through adaptive specialization, species that cache food have better spatial memory and a relatively larger hippocampus than their non-caching relatives. Critics of this approach, dubbed neuroecology, maintain that neither of these hypotheses has been confirmed. Here, we review the evidence pertaining to a correlation between food-storing capability and the relative volume of the hippocampus. Hippocampal volume has been related to food-storing behaviour in comparisons between species, within species, or within individuals, but the evidence is not consistent. There are several possible reasons for this inconsistency, including: (1) food-hoarding birds may not always use memory for retrieval, (2) there may be systematic differences between data from North American and Eurasian species that affect the analysis, and (3) sample sizes have in many cases been too small. In addition, both the independent variable (degree of food-hoarding specialization) and the dependent variable (relative volume of the hippocampus) are not clearly and consistently defined. Alternatively, it is possible that the neuroecological hypothesis is false. Systematic empirical research is necessary to determine whether or not food-storing birds have evolved adaptive specializations in brain and cognition.     

Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds

Maintaining cognitive processes comes with neurological costs. Thus, enhanced cognition and its underlying neural mechanisms should change in response to environmental pressures. Indeed, recent evidence suggests that variation in spatially based cognitive abilities is reflected in the morphology of the hippocampus (Hp), the region of the brain involved in spatial memory. Moreover, recent work on this region establishes a dynamic link between brain plasticity and cognitive experiences both across populations and within individuals. However, the mechanisms involved in neurological changes as a result of differential space use and the reversibility of such effects are unknown. Using a house sparrow (Passer domesticus ) model, we experimentally manipulated the space available to birds, testing the hypothesis that reductions in dendritic branching is associated with reduced Hp volume and that such reductions in volume are reversible. We found that reduced spatial availability associated with captivity had a profound and significant reduction in sparrow hippocampal volumes, which was highly correlated with the total length of dendrites in the region. This result suggests that changes to the dendritic structure of neurons may, in part, explain volumetric reductions in region size associated with captivity. In addition, small changes in available space even within captivity produced significant changes in the spine structure on Hp dendrites. These reductions were reversible following increased spatial opportunities. Overall, these results are consistent with the hypothesis that reductions to the Hp in captivity, often assumed to reflect a deleterious process, may be adaptive and a consequence of the trade‐off between cognitive and energetic demands. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 93–101, 2017     

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.     

The history of scatter hoarding studies

In this review, I will present an overview of the development of the field of scatter hoarding studies. Scatter hoarding is a conspicuous behaviour and it has been observed by humans for a long time. Apart from an exceptional experimental study already published in 1720, it started with observational field studies of scatter hoarding birds in the 1940s. Driven by a general interest in birds, several ornithologists made large-scale studies of hoarding behaviour in species such as nutcrackers and boreal titmice. Scatter hoarding birds seem to remember caching locations accurately, and it was shown in the 1960s that successful retrieval is dependent on a specific part of the brain, the hippocampus. The study of scatter hoarding, spatial memory and the hippocampus has since then developed into a study system for evolutionary studies of spatial memory. In 1978, a game theoretical paper started the era of modern studies by establishing that a recovery advantage is necessary for individual hoarders for the evolution of a hoarding strategy. The same year, a combined theoretical and empirical study on scatter hoarding squirrels investigated how caches should be spaced out in order to minimize cache loss, a phenomenon sometimes called optimal cache density theory. Since then, the scatter hoarding paradigm has branched into a number of different fields: (i) theoretical and empirical studies of the evolution of hoarding, (ii) field studies with modern sampling methods, (iii) studies of the precise nature of the caching memory, (iv) a variety of studies of caching memory and its relationship to the hippocampus. Scatter hoarding has also been the subject of studies of (v) coevolution between scatter hoarding animals and the plants that are dispersed by these.     

The ecological relevance of sleep: the trade-off between sleep,memory and energy conservation

All animals in which sleep has been studied express signs of sleep-like behaviour, suggesting that sleep must have some fundamental functions that are sustained by natural selection. Those functions, however, are still not clear. Here, we examine the ecological relevance of sleep from the perspective of behavioural trade-offs that might affect fitness. Specifically, we highlight the advantage of using food-caching animals as a system in which a conflict might occur between engaging in sleep for memory/learning and hypothermia/torpor to conserve energy. We briefly review the evidence for the importance of sleep for memory, the importance of memory for food-caching animals and the conflicts that might occur between sleep and energy conservation in these animals. We suggest that the food-caching paradigm represents a naturalistic and experimentally practical system that provides the opportunity for a new direction in sleep research that will expand our understanding of sleep, especially within the context of ecological and evolutionary processes.