Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms, Behavioral Constraints, and Evolutionary Context.

Unlike birds and mammals, reptiles are commonly thought to possess only the most rudimentary means of interacting with their environments, reflexively responding to sensory information to the near exclusion of higher cognitive function. However, reptilian brains, though structurally somewhat different from those of mammals and birds, use many of the same cellular and molecular processes to support complex behaviors in homologous brain regions. Here, the neurological mechanisms supporting reptilian cognition are reviewed, focusing specifically on spatial cognition and the hippocampus. These processes are compared to those seen in mammals and birds within an ecologically and evolutionarily relevant context. By viewing reptilian cognition through an integrative framework, a more robust understanding of reptile cognition is gleaned. Doing so yields a broader view of the evolutionarily conserved molecular and cellular mechanisms that underlie cognitive function and a better understanding of the factors that led to the evolution of complex cognition.

Of molecules, memories and migration: M1 acetylcholine receptors facilitate spatial memory formation and recall during migratory navigation.

Many animals use complex cognitive processes, including the formation and recall of memories, for successful navigation. However, the developmental and neurological processes underlying these cognitive aspects of navigation are poorly understood. To address the importance of the formation and recollection of memories during navigation, we pharmacologically manipulated turtles (Chrysemys picta) that navigate long distances using precise, complex paths learned during a juvenile critical period. We treated freely navigating turtles both within and outside of their critical learning period with a specific M1 acetylcholine receptor antagonist, a drug known to disrupt spatial cognition. Experienced adult turtles lost all navigational ability under the influence of the drug, while naive juveniles navigated successfully. We retested these same juveniles the following year (after they had passed their critical period). The juveniles that initially navigated successfully under the influence of the antagonist (but were unable to form spatial memories) were unable to do so subsequently. However, the control animals (who had the opportunity to form memories previously) exhibited typical navigational precision. These results suggest that the formation of spatial memories for navigation occur during a critical period, and successful navigation after the critical period is dependent upon the recall of such memories.

Pharmacological evidence is consistent with a prominent role of spatial memory in complex navigation.

The ability to learn about the spatial environment plays an important role in navigation, migration, dispersal, and foraging. However, our understanding of both the role of cognition in the development of navigation strategies and the mechanisms underlying these strategies is limited. We tested the hypothesis that complex navigation is facilitated by spatial memory in a population of Chrysemys picta that navigate with extreme precision (±3.5 m) using specific routes that must be learned prior to age three. We used scopolamine, a muscarinic acetylcholine receptor antagonist, to manipulate the cognitive spatial abilities of free-living turtles during naturally occurring overland movements. Experienced adults treated with scopolamine diverted markedly from their precise navigation routes. Naive juveniles lacking experience (and memory) were not affected by scopolamine, and thereby served as controls for perceptual or non-spatial cognitive processes associated with navigation. Further, neither adult nor juvenile movement was affected by methylscopolamine, a form of scopolamine that does not cross the blood-brain barrier, a control for the peripheral effects of scopolamine. Together, these results are consistent with a role of spatial cognition in complex navigation and highlight a cellular mechanism that might underlie spatial cognition. Overall, our findings expand our understanding of the development of complex cognitive abilities of vertebrates and the neurological mechanisms of navigation.

Chickadees with bigger brains have smaller digestive tracts: a multipopulation comparison.

The factors leading to the evolution of large brain size remain controversial. Brains are metabolically expensive and larger brains demand higher maintenance costs. The expensive-tissue hypothesis suggests that when selection favors larger brains, evolutionary changes in brain size can occur without an overall increase in energetic costs when brain size represents a trade-off with the size of other expensive tissues, such as the digestive tract. Still, support for this hypothesis is equivocal. We compared mean brain mass, digestive tract mass (stomach and gut) and heart mass in 9 populations of black-capped chickadees along a gradient of winter climate severity. Mean brain mass and telencephalon volume showed significant population variation with larger brains associated with harsher winter conditions. Mean population brain mass and telencephalon volume were also negatively related to both stomach and gut mass. Mean population heart mass, on the other hand, was not significantly associated with either mean brain mass or winter climate severity. Mean brain mass was negatively associated with body mass, with chickadees from harsher environments being smaller but having larger brains and smaller digestive tracts. Our results are consistent with the expensive-tissue hypothesis, and suggest that a harsher winter climate might favor larger brains, which might be associated with a reduction in size of the digestive tract. These findings could potentially be a result of population differences in the winter climate diet related to the perishability of more efficient invertebrate-based food caches.

Reptilian cognition.

Tim Roth and Aaron Krochmal discuss reptile cognition in an integrative and comparative light.

Australian magpies.

Robin D. Johnsson and colleagues introduce Australian magpies, which are not actually magpies.

Learning and memory in hybrid migratory songbirds: cognition as a reproductive isolating barrier across seasons.

Hybrid zones can be used to identify traits that maintain reproductive isolation and contribute to speciation. Cognitive traits may serve as post-mating reproductive isolating barriers, reducing the fitness of hybrids if, for example, misexpression occurs in hybrids and disrupts important neurological mechanisms. We tested this hypothesis in a hybrid zone between two subspecies of Swainson's thrushes (Catharus ustulatus) using two cognitive tests-an associative learning spatial test and neophobia test. We included comparisons across the sexes and seasons (spring migration and winter), testing if hybrid females performed worse than males (as per Haldane's rule) and if birds (regardless of ancestry or sex) performed better during migration, when they are building navigational maps and encountering new environments. We documented reduced cognitive abilities in hybrids, but this result was limited to males and winter. Hybrid females did not perform worse than males in either season. Although season was a significant predictor of performance, contrary to our prediction, all birds learned faster during the winter. The hypothesis that cognitive traits could serve as post-mating isolating barriers is relatively new; this is one of the first tests in a natural hybrid zone and non-food-caching species. We also provide one of the first comparisons of cognitive abilities between seasons. Future neurostructural and neurophysiological work should be used to examine mechanisms underlying our behavioral observations.

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.

Evidence for long-term spatial memory in a parid.

Many animals use spatial memory. Although much work has examined the accuracy of spatial memory, few studies have explicitly focused on its longevity. The importance of long-term spatial memory for foraging has been demonstrated in several cases. However, the importance of such long-term memory for all animals is unclear. In this study, we present the first evidence that a parid species (the black-capped chickadee, Poecile atricapillus) can remember the location of a single food item for at least 6 months under an associative-learning spatial memory paradigm with multiple reinforcements. We did not detect a significant difference in memory longevity between two populations of chickadees shown previously to differ in short-term spatial memory and hippocampal morphology, an area of the brain involved in spatial memory. Our study showed that small birds such as parids can maintain spatial memories for long periods, a feat shown previously only in corvids. Moreover, we were able to demonstrate this longevity within the context of only 16 repeated trials. We speculate that this ability may potentially be useful in relocating caches if reinforced by repeated visits. Future studies are necessary to test whether our results were specifically due to multiple reinforcements of the food-containing location and whether parids may have similar memory longevity during food-caching experiences in the wild.

Variation in brain regions associated with fear and learning in contrasting climates.

In environments where resources are difficult to obtain and enhanced cognitive capabilities might be adaptive, brain structures associated with cognitive traits may also be enhanced. In our previous studies, we documented a clear and significant relationship among environmental conditions, memory and hippocampal structure using ten populations of black-capped chickadees (Poecile atricapillus) over a large geographic range. In addition, focusing on just the two populations from the geographical extremes of our large-scale comparison, Alaska and Kansas, we found enhanced problem-solving capabilities and reduced neophobia in a captive-raised population of black-capped chickadees originating from the energetically demanding environment (Alaska) relative to conspecifics from the milder environment (Kansas). Here, we focused on three brain regions, the arcopallium (AP), the nucleus taeniae of the amygdala and the lateral striatum (LSt), that have been implicated to some extent in aspects of these behaviors in order to investigate whether potential differences in these brain areas may be associated with our previously detected differences in cognition. We compared the variation in neuron number and volumes of these regions between these populations, in both wild-caught birds and captive-raised individuals. Consistent with our behavioral observations, wild-caught birds from Kansas had a larger AP volume than their wild-caught conspecifics from Alaska, which possessed a higher density of neurons in the LSt. However, there were no other significant differences between populations in the wild-caught and captive-raised groups. Interestingly, individuals from the wild had larger LSt and AP volumes with more neurons than those raised in captivity. Overall, we provide some evidence that population-related differences in problem solving and neophobia may be associated with differences in volume and neuron numbers of our target brain regions. However, the relationship is not completely clear, and our study raises numerous questions about the relationship between the brain and behavior, especially in captive animals.

Homeostatic regulation of NREM sleep, but not REM sleep, in Australian magpies.

STUDY OBJECTIVES: We explore non-rapid eye movement (NREM) and rapid eye movement (REM) sleep homeostasis in Australian magpies (Cracticus tibicen tyrannica). We predicted that magpies would recover lost sleep by spending more time in NREM and REM sleep, and by engaging in more intense NREM sleep as indicated by increased slow-wave activity (SWA). METHODS: Continuous 72-h recordings of EEG, EMG, and tri-axial accelerometry, along with EEG spectral analyses, were performed on wild-caught Australian magpies housed in indoor aviaries. Australian magpies were subjected to two protocols of night-time sleep deprivation: full 12-h night (n = 8) and first 6-h half of the night (n = 5), which were preceded by a 36-h baseline recording and followed by a 24-h recovery period. RESULTS: Australian magpies recovered from lost NREM sleep by sleeping more, with increased NREM sleep consolidation, and increased SWA during recovery sleep. Following 12-h of night-time sleep loss, magpies also showed reduced SWA the following night after napping more during the recovery day. Surprisingly, the magpies did not recover any lost REM sleep. CONCLUSIONS: Only NREM sleep is homeostatically regulated in Australian magpies with the level of SWA reflecting prior sleep/wake history. The significance of emerging patterns on the apparent absence of REM sleep homeostasis, now observed in multiple species, remains unclear.

Sleep loss impairs cognitive performance and alters song output in Australian magpies.

Sleep maintains optimal brain functioning to facilitate behavioural flexibility while awake. Owing to a historical bias towards research on mammals, we know comparatively little about the role of sleep in facilitating the cognitive abilities of birds. We investigated how sleep deprivation over the full-night (12 h) or half-night (6 h) affects cognitive performance in adult Australian magpies (Cracticus tibicen), relative to that after a night of undisturbed sleep. Each condition was preceded and followed by a baseline and recovery night of sleep, respectively. Prior to each treatment, birds were trained on an associative learning task; on the day after experimental treatment (recovery day), birds were tested on a reversal learning task. To glean whether sleep loss affected song output, we also conducted impromptu song recordings for three days. Ultimately, sleep-deprived magpies were slower to attempt the reversal learning task, less likely to perform and complete the task, and those that did the test performed worse than better-rested birds. We also found that sleep-deprived magpies sang longer yet fewer songs, shifted crepuscular singing to mid-day, and during the post-recovery day, song frequency bandwidth narrowed. These results collectively indicate that sleep loss impairs motivation and cognitive performance, and alters song output, in a social adult songbird.

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.

Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.).

It has been hypothesized that individuals who have higher demands for spatially based behaviours should show increases in hippocampal attributes. Some avian species have been shown to use a spatially based representation of their environment during migration. Further, differences in hippocampal attributes have been shown between migratory and non-migratory subspecies as well as between individuals with and without migratory experience (juveniles versus adults). We tested whether migratory behaviour might also be associated with increased hippocampal neurogenesis, and whether potential differences track previously reported differences in hippocampal attributes between a migratory (Zonotrichia leucophrys gambelii) and non-migratory subspecies (Z. l. nuttalli) of white-crowned sparrows. We found that non-migratory adults had relatively fewer numbers of immature hippocampal neurons than adult migratory birds, while adult non-migrants had a lower density of new hippocampal neurons than adult and juvenile migratory birds and juvenile non-migratory birds. Our results suggest that neurogenesis decreases with age, as juveniles, regardless of migratory status, exhibit similar and higher levels of neurogenesis than non-migratory adults. However, our results also suggest that adult migrants may either seasonally increase or maintain neurogenesis levels comparable to those found in juveniles. Our results thus suggest that migratory behaviour in adults is associated with maintained or increased neurogenesis and the differential production of new neurons may be the mechanism underpinning changes in the hippocampal architecture between adult migratory and non-migratory birds.

Learning capabilities enhanced in harsh environments: a common garden approach.

Previous studies have suggested that the ability to inhabit harsh environments may be linked to advanced learning traits. However, it is not clear if individuals express such traits as a consequence of experiencing challenging environments or if these traits are inherited. To assess the influence of differential selection pressures on variation in aspects of cognition, we used a common garden approach to examine the response to novelty and problem-solving abilities of two populations of black-capped chickadees (Poecile atricapillus). These populations originated from the latitudinal extremes of the species's range, where we had previously demonstrated significant differences in memory and brain morphology in a multi-population study. We found that birds from the harsh northern population, where selection for cognitive abilities is expected to be high, significantly outperformed conspecifics from the mild southern population. Our results imply differences in cognitive abilities that may be inherited, as individuals from both populations were raised in and had experienced identical environmental conditions from 10 days of age. Although our data suggest an effect independent of experience, we cannot rule out maternal effects or experiences within the nest prior to day 10 with our design. Nevertheless, our results support the idea that environmental severity may be an important factor in shaping certain aspects of cognition.

Ecologically relevant spatial memory use modulates hippocampal neurogenesis.

The adult hippocampus in birds and mammals undergoes neurogenesis and the resulting new neurons appear to integrate structurally and functionally into the existing neural architecture. However, the factors underlying the regulation of new neuron production is still under scrutiny. In recent years, the concept that spatial memory affects adult hippocampal neurogenesis has gained acceptance, although results attempting to causally link memory use to neurogenesis remain inconclusive, possibly owing to confounds of motor activity, task difficulty or training for the task. Here, we show that ecologically relevant, spatial memory-based experiences of food caching and retrieving directly affect hippocampal neurogenesis in mountain chickadees (Poecile gambeli). We found that restricting memory experiences in captivity caused significantly lower rates of neurogenesis, as determined by doublecortin expression, compared with captive individuals provided with such experiences. However, neurogenesis rates in both groups of captive birds were still greatly lower than those in free-ranging conspecifics. These findings show that ecologically relevant spatial memory experiences can directly modulate neurogenesis, separate from other confounds that may also independently affect neurogenesis.

Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison.

Environmental conditions may provide specific demands for memory, which in turn may affect specific brain regions responsible for memory function. For food-caching animals, in particular, spatial memory appears to be important because it may have a direct effect on fitness via the accuracy of cache retrieval. Animals living in more harsh environments should rely more on cached food, and thus theoretically should have better memory to support cache retrieval, which may be crucial for survival. Consequently, animals in harsh environments may benefit from more neurons within a larger hippocampus (Hp), a part of the brain involved in spatial memory. Here, we present the first large-scale test of the hypothesis that Hp structure is related to the severity of the environment within a single food-caching species (the black-capped chickadee, Poecile atricapillus) with a large range encompassing a great diversity of climatic conditions. Hp size in birds collected at five locations along a gradient of environmental harshness from Alaska to Kansas ranked perfectly with climatic severity. Birds from more harsh northern climates (defined by lower ambient temperature, shorter day length and more snow cover) had significantly larger Hp volumes and more Hp neurons (both relative to telencephalon volume) than those from more mild southern latitudes. Environmental pressures therefore seem capable of influencing specific brain regions independently, which may result in enhanced memory, and hence survival, in harsh climates.

Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees.

The complexity of an animal's physical environment is known to affect the hippocampus. Captivity may affect hippocampal anatomy and this may be attributable to the limited opportunities for memory-based experiences. This has tangential support, in that differential demands on memory can mediate changes in the hippocampus. What remains unclear is whether captivity directly affects hippocampal architecture and whether providing memory-based experiences in captivity can maintain hippocampal attributes comparable to wild-caught conspecifics. Using food-caching mountain chickadees (Poecile gambeli), we found that wild-caught individuals had larger hippocampal volumes relative to the rest of the telencephalon than captive birds with or without memory-based food-caching experiences, whereas there were no differences in neuron numbers or telencephalon volume. Also, there were no significant differences in relative hippocampal volume or neuron numbers between the captive birds with or without memory-based experiences. Our results demonstrate that captivity reduces hippocampal volume relative to the remainder of the telencephalon, but not at the expense of neuron numbers. Further, memory-based experiences in captivity may not be sufficient to maintain hippocampal volume comparable to wild-caught counterparts.

Flexible cue use in food-caching birds.

An animal's memory may be limited in capacity, which may result in competition among available memory cues. If such competition exists, natural selection may favor prioritization of different memory cues based on cue reliability and on associated differences in the environment and life history. Food-caching birds store numerous food items and appear to rely on memory to retrieve caches. Previous studies suggested that caching species should always prioritize spatial cues over non-spatial cues when both are available, because non-spatial cues may be unreliable in a changing environment; however, it remains unclear whether non-spatial cues should always be ignored when spatial cues are available. We tested whether mountain chickadees (Poecile gambeli), a food-caching species, prioritize memory for spatial cues over color cues when relocating previously found food in an associative learning task. In training trials, birds were exposed to food in a feeder where both spatial location and color were associated. During subsequent unrewarded test trials, color was dissociated from spatial location. Chickadees showed a significant pattern of inspecting feeders associated with correct color first, prior to visiting correct spatial locations. Our findings argue against the hypothesis that the memory of spatial cues should always take priority over any non-spatial cues, including color cues, in food-caching species, because in our experiment mountain chickadees chose color over spatial cues. Our results thus suggest that caching species may be more flexible in cue use than previously thought, possibly dependent upon the environment and complexity of available cues.

Biases in measuring the brain: the trouble with the telencephalon.

When correlating behavior with particular brain regions thought responsible for the behavior, a different region of the brain is usually measured as a control region. This technique is often used to relate spatial processes with the hippocampus, while concomitantly controlling for overall brain changes by measuring the remainder of the telencephalon. We have identified two methods in the literature (the HOM and TTM) that estimate the volume of the telencephalon, although the majority of studies are ambiguous regarding the method employed in measuring the telencephalon. Of these two methods, the HOM might produce an artificial correlation between the telencephalon and the hippocampus, and this bias could result in a significant overestimation of the relative hippocampal volume and a significant underestimation of the telencephalon volume, both of which are regularly used in large comparative analyses. We suggest that future studies should avoid this method and all studies should explicitly delineate the procedures used when estimating brain volumes.