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.

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.

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.

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.

Hybrid chickadees are deficient in learning and memory.

Identifying the phenotypes underlying postzygotic reproductive isolation is crucial for fully understanding the evolution and maintenance of species. One potential postzygotic isolating barrier that has rarely been examined is learning and memory ability in hybrids. Learning and memory are important fitness-related traits, especially in scatter-hoarding species, where accurate retrieval of hoarded food is vital for winter survival. Here, we test the hypothesis that learning and memory ability can act as a postzygotic isolating barrier by comparing these traits among two scatter-hoarding songbird species, black-capped (Poecile atricapillus) and Carolina chickadees (Poecile carolinensis), and their naturally occurring hybrids. In an outdoor aviary setting, we find that hybrid chickadees perform significantly worse on an associative learning spatial task and are worse at solving a novel problem compared to both parental species. Deficiencies in learning and memory abilities could therefore contribute to postzygotic reproductive isolation between chickadee species. Given the importance of learning and memory for fitness, our results suggest that these traits may play an important, but as yet overlooked, role in postzygotic reproductive isolation.

Increased Testosterone Decreases Medial Cortical Volume and Neurogenesis in Territorial Side-Blotched Lizards (Uta stansburiana).

Variation in an animal's spatial environment can induce variation in the hippocampus, an area of the brain involved in spatial cognitive processing. Specifically, increased spatial area use is correlated with increased hippocampal attributes, such as volume and neurogenesis. In the side-blotched lizard (Uta stansburiana), males demonstrate alternative reproductive tactics and are either territorial-defending large, clearly defined spatial boundaries-or non-territorial-traversing home ranges that are smaller than the territorial males' territories. Our previous work demonstrated cortical volume (reptilian hippocampal homolog) correlates with these spatial niches. We found that territorial holders have larger medial cortices than non-territory holders, yet these differences in the neural architecture demonstrated some degree of plasticity as well. Although we have demonstrated a link among territoriality, spatial use, and brain plasticity, the mechanisms that underlie this relationship are unclear. Previous studies found that higher testosterone levels can induce increased use of the spatial area and can cause an upregulation in hippocampal attributes. Thus, testosterone may be the mechanistic link between spatial area use and the brain. What remains unclear, however, is if testosterone can affect the cortices independent of spatial experiences and whether testosterone differentially interacts with territorial status to produce the resultant cortical phenotype. In this study, we compared neurogenesis as measured by the total number of doublecortin-positive cells and cortical volume between territorial and non-territorial males supplemented with testosterone. We found no significant differences in the number of doublecortin-positive cells or cortical volume among control territorial, control non-territorial, and testosterone-supplemented non-territorial males, while testosterone-supplemented territorial males had smaller medial cortices containing fewer doublecortin-positive cells. These results demonstrate that testosterone can modulate medial cortical attributes outside of differential spatial processing experiences but that territorial males appear to be more sensitive to alterations in testosterone levels compared with non-territorial males.

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.

Using Pharmacological Manipulation and High-precision Radio Telemetry to Study the Spatial Cognition in Free-ranging Animals.

An animal's ability to perceive and learn about its environment plays a key role in many behavioral processes, including navigation, migration, dispersal and foraging. However, the understanding of the role of cognition in the development of navigation strategies and the mechanisms underlying these strategies is limited by the methodological difficulties involved in monitoring, manipulating the cognition of, and tracking wild animals. This study describes a protocol for addressing the role of cognition in navigation that combines pharmacological manipulation of behavior with high-precision radio telemetry. The approach uses scopolamine, a muscarinic acetylcholine receptor antagonist, to manipulate cognitive spatial abilities. Treated animals are then monitored with high frequency and high spatial resolution via remote triangulation. This protocol was applied within a population of Eastern painted turtles (Chrysemys picta) that has inhabited seasonally ephemeral water sources for ~100 years, moving between far-off sources using precise (± 3.5 m), complex (i.e., non-linear with high tortuosity that traverse multiple habitats), and predictable routes learned before 4 years of age. This study showed that the processes used by these turtles are consistent with spatial memory formation and recall. Together, these results are consistent with a role of spatial cognition in complex navigation and highlight the integration of ecological and pharmacological techniques in the study of cognition and navigation.

Sleep Ecophysiology: Integrating Neuroscience and Ecology.

Here, we propose an original approach to explain one of the great unresolved questions in animal biology: what is the function of sleep? Existing ecological and neurological approaches to this question have become roadblocks to an answer. Ecologists typically treat sleep as a simple behavior, instead of a heterogeneous neurophysiological state, while neuroscientists generally fail to appreciate the critical insights offered by the consideration of ecology and evolutionary history. Redressing these shortfalls requires cross-disciplinary integration. By bringing together aspects of behavioral ecology, evolution, and conservation with neurophysiology, we can achieve a more comprehensive understanding of sleep, including its implications for adaptive waking behavior and fitness.

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.

Thinking about Change: An Integrative Approach for Examining Cognition in a Changing World.

We are currently experiencing shifts in climate at rates not previously recorded. One important aspect of this change is a tendency toward extremes--extremes in temperature and moisture, both within and among years. Numerous studies focus on the physiological consequences of environmental change, especially in terms of ectothermic taxa's thermal regime and use of habitat. For many species, though, cognitive responses may be a means of response to environmental perturbation. However, the effects of environmental change on the general mechanisms of cognitive processes and their implications for larger phenomena are seldom examined. Moreover, at a larger scale, we do not fully understand the features of the environment that might select for cognitive enhancements or their mechanisms, making us unable to accurately predict which species might experience the most severe response to environmental change and in which environments. This symposium brought together scientists from numerous disciplines to examine the role of cognition in how organisms cope with changing environments. We cover topics from the perspectives of the physiological mechanisms underlying and driving cognition to the complexity of individual behavioral responses in changing environments to emergent large-scale processes influencing species' abilities to respond to such change. Our ultimate goals are to explore how animals use cognition to cope with rapid environmental change, how such coping mechanisms "scale up" to affect ecological and evolutionary patterns, and how we might determine which features of the environment have been (and will become) most important for the conservation of biodiversity.

Potential Mechanisms Driving Population Variation in Spatial Memory and the Hippocampus in Food-caching Chickadees.

Harsh environments and severe winters have been hypothesized to favor improvement of the cognitive abilities necessary for successful foraging. Geographic variation in winter climate, then, is likely associated with differences in selection pressures on cognitive ability, which could lead to evolutionary changes in cognition and its neural mechanisms, assuming that variation in these traits is heritable. Here, we focus on two species of food-caching chickadees (genus Poecile), which rely on stored food for survival over winter and require the use of spatial memory to recover their stores. These species also exhibit extensive climate-related population level variation in spatial memory and the hippocampus, including volume, the total number and size of neurons, and adults' rates of neurogenesis. Such variation could be driven by several mechanisms within the context of natural selection, including independent, population-specific selection (local adaptation), environment experience-based plasticity, developmental differences, and/or epigenetic differences. Extensive data on cognition, brain morphology, and behavior in multiple populations of these two species of chickadees along longitudinal, latitudinal, and elevational gradients in winter climate are most consistent with the hypothesis that natural selection drives the evolution of local adaptations associated with spatial memory differences among populations. Conversely, there is little support for the hypotheses that environment-induced plasticity or developmental differences are the main causes of population differences across climatic gradients. Available data on epigenetic modifications of memory ability are also inconsistent with the observed patterns of population variation, with birds living in more stressful and harsher environments having better spatial memory associated with a larger hippocampus and a larger number of hippocampal neurons. Overall, the existing data are most consistent with the hypothesis that highly predictable differences in winter climate drive the evolution and maintenance of differences among populations both in cognition and in the brain via local adaptations, at least in food-caching parids.

The role of age-specific learning and experience for turtles navigating a changing landscape.

The severity of the environment often influences animal cognition [1-6], as does the rate of change within that environment [7-10]. Rapid alteration of habitat places limitations on basic resources such as energy, water, nesting sites, and refugia [8, 10]. How animals respond to these situations provides insight into the mechanisms of cognition and the role of behavior in adaptation [11-13]. We tested the hypothesis that learning plays a role in the navigation of the painted turtle (Chrysemys picta) within a model of environmental change. We radiotracked experienced and naive turtles at different developmental stages from two different populations as they sought out new habitats when their pond was destroyed. Our data suggest that the ability of turtles to navigate is facilitated in part by experience during a critical period. Resident adults repeatedly used specific routes with exceptional precision, while translocated adults failed to find water. Naive juveniles (1-3 years old) from both populations used the same paths taken by resident adults; the ability to follow paths was lost by age 4. We also used laboratory behavioral assays to examine the possible cues facilitating this precise navigation. Turtles responded to manipulation of the local ultraviolet environment, but not the olfactory environment. This is the first evidence to suggest that learning during a critical period may be important for how animals respond to changing environments. Our work emphasizes the need for the examination of learning in navigation and the breadth of critical learning periods across vertebrates.

Turtles outsmart rapid environmental change: The role of cognition in navigation.

Animals inhabiting changing environments show high levels of cognitive plasticity. Cognition may be a means by which animals buffer the impact of environmental change. However, studies examining the evolution of cognition seldom compare populations where change is rapid and selection pressures are strong. We investigated this phenomenon by radiotracking experienced and naïve Eastern painted turtles (Chrysemys picta) as they sought new habitats when their pond was drained. Resident adults repeatedly used specific routes to permanent water sources with exceptional precision, while adults translocated to the site did not. Naïve 1-3 y olds from both populations used the paths taken by resident adults, an ability lost by age 4. Experience did not, however, influence the timing of movement or the latency to begin navigation. This suggests that learning during a critical period may be important for how animals respond to changing environments, highlighting the importance of incorporating cognition into conservation.

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.

Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards.

Differences in an animal's spatial environment can have dramatic effects on the hippocampus, an area of the brain involved with spatial processing. Animals in spatially impoverished environments have decreased hippocampal attributes. However, we do not know if differences in the spatial environment differentially interact with territorial status, which also covaries with hippocampal attributes. Here, we asked whether territoriality and differential spatial-area use interact to generate different effects on cortical attributes (reptilian hippocampal homologue) in lizards. We compared medial and dorsal cortical attributes between territorial and nonterritorial morphotypes of side-blotched lizards, Uta stansburiana, in larger versus smaller (i.e., spatially impoverished) enclosures. We found that territorial males had increased neurogenesis rates in their medial cortices in larger enclosures when compared with their siblings in smaller enclosures; nonterritorial males had low levels of neurogenesis regardless of enclosure size. Enclosure size had no significant effect on cortical volumes or the total number of neurons in either cortical region. These results suggest that territorial morphotypes may be more sensitive to changes in the spatial environment, thus leading to increases in regulation of neurogenesis in the face of increased spatial processing and physical activity demands.

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.