The effects of early-life and intergenerational stress on the brain.

Stress experienced during ontogeny can have profound effects on the adult phenotype. However, stress can also be experienced intergenerationally, where an offspring's phenotype can be moulded by stress experienced by the parents. Although early-life and intergenerational stress can alter anatomy, physiology, and behaviour, nothing is known about how these stress contexts interact to affect the neural phenotype. Here, we examined how early-life and intergenerational stress affect the brain in eastern fence lizards (Sceloporus undulatus). Some lizard populations co-occur with predatory fire ants, and stress from fire ant attacks exerts intergenerational physiological and behavioural changes in lizards. However, it is unclear if intergenerational stress, or the interaction between intergenerational and early-life stress, modulates the brain. To test this, we captured gravid females from fire ant invaded and uninvaded populations, and subjected offspring to three early-life stress treatments: (1) fire ant attack, (2) corticosterone, or (3) a control. Corticosterone and fire ant attack decreased some aspects of the neural phenotype while population of origin and the interaction of early-life stress and population had no effects on the brain. These results suggest that early-life stressors may better predict adult brain variation than intergenerational stress in this species.

A reflection on noncognitive factors affecting spatial cognitive testing: Examples from nonmodel species.

Probing for spatial cognitive processes in model rodent species has a long history in the psychological literature, with well-established protocols and paradigms successfully revealing the mechanisms underlying spatial learning and memory. There has also been much interest in examining the ecological and evolutionary context of spatial cognition, with a focus on how selection has molded spatial cognitive abilities in nonmodel species, how spatial cognitive traits vary across species, the neural mechanisms underlying spatial cognitive abilities, and the fitness outcomes of spatial cognition. Behavioral ecologists have been able to take advantage of paradigms from experimental psychology's rich history of spatial cognitive testing for use in nonmodel species. However, as the field advances, it is important to highlight noncognitive factors that can impact performance on spatial cognitive tasks (e.g., motivation to perform the task, switching navigational strategies, variation across protocols, ecological relevance of the task), as these factors may explain discrepancies in findings among some studies. This review highlights how these noncognitive factors can differentially modulate performance on spatial cognitive tests in different nonmodel species. Accounting for these factors when creating protocols and paradigms allows for a more nuanced approach with more explanatory power when probing for spatial cognitive abilities in nonmodel species. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Higher Rate of Male Sexual Displays Correlates with Larger Ventral Posterior Amygdala Volume and Neuron Soma Volume in Wild-Caught Common Side-Blotched Lizards, Uta stansburiana.

Several areas of the vertebrate brain are involved in facilitating and inhibiting the production of sexual behaviors and displays. In the laboratory, a higher rate of sexual displays is correlated with a larger ventral posterior amygdala (VPA), an area of the brain involved in the expression of sexual display behaviors, as well as larger VPA neuronal somas. However, it remains unclear if individuals in the field reflect similar patterns, as there are likely many more selective pressures in the field that may also modulate the VPA architecture. In this study, we examined variation in VPA volume and neuron soma volume in wild-caught common side-blotched lizards (Uta stansburiana) from two different populations. In a population from Nevada, males experience high predation pressure and have decreased sexual display rates during the breeding season, whereas a population in Oregon has lower levels of predation and higher rates of male sexual displays. We found that wild-caught males from the population with lower display rates also exhibited decreased VPA volume and VPA neuron cell soma volume, which may suggest that decreased display rate, possibly due to increased predation rate, covaries with VPA attributes.

Seasonal variation in gonadal hormones, spatial cognition, and hippocampal attributes: More questions than answers.

A large body of research has been dedicated to understanding the factors that modulate spatial cognition and attributes of the hippocampus, a highly plastic brain region that underlies spatial processing abilities. Variation in gonadal hormones impacts spatial memory and hippocampal attributes in vertebrates, although the direction of the effect has not been entirely consistent. To add complexity, individuals in the field must optimize fitness by coordinating activities with the appropriate environmental cues, and many of these behaviors are correlated tightly with seasonal variation in gonadal hormone release. As such, it remains unclear if the relationship among systemic gonadal hormones, spatial cognition, and the hippocampus also exhibits seasonal variation. This review presents an overview of the relationship among gonadal hormones, the hippocampus, and spatial cognition, and how the seasonal release of gonadal hormones correlates with seasonal variation in spatial cognition and hippocampal attributes. Additionally, this review presents other neuroendocrine mechanisms that may be involved in modulating the relationship among seasonality, gonadal hormone release, and the hippocampus and spatial cognition, including seasonal rhythms of steroid hormone binding globulins, neurosteroids, sex steroid hormone receptor expression, and hormone interactions. Here, endocrinology, ecology, and behavioral neuroscience are brought together to present an overview of the research demonstrating the mechanistic effects of systemic gonadal hormones on spatial cognition and the hippocampus, while, at a functional level, superimposing seasonal effects to examine ecologically-relevant circannual changes in gonadal hormones and spatial behaviors.

Broadening the functional and evolutionary understanding of postnatal neurogenesis using reptilian models.

The production of new neurons in the brains of adult animals was first identified by Altman and Das in 1965, but it was not until the late 20th century when methods for visualizing new neuron production improved that there was a dramatic increase in research on neurogenesis in the adult brain. We now know that adult neurogenesis is a ubiquitous process that occurs across a wide range of taxonomic groups. This process has largely been studied in mammals; however, there are notable differences between mammals and other taxonomic groups in how, why and where new neuron production occurs. This Review will begin by describing the processes of adult neurogenesis in reptiles and identifying the similarities and differences in these processes between reptiles and model rodent species. Further, this Review underscores the importance of appreciating how wild-caught animals vary in neurogenic properties compared with laboratory-reared animals and how this can be used to broaden the functional and evolutionary understanding of why and how new neurons are produced in the adult brain. Studying variation in neural processes across taxonomic groups provides an evolutionary context to adult neurogenesis while also advancing our overall understanding of neurogenesis and brain plasticity.

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.

Variation in behavioral engagement during an active learning activity leads to differential knowledge gains in college students.

There are many pedagogical techniques used by educators in higher education; however, some techniques and activities have been shown to be more beneficial to student learning than others. Research has demonstrated that active learning and learning in which students cognitively engage with the material in a multitude of ways result in better understanding and retention. The aim of the present study was to determine which of three pedagogical techniques led to improvement in learning and retention in undergraduate college students. Subjects partook in one of three different types of pedagogical engagement: hands-on learning with a model, observing someone else manipulate the model, and traditional lecture-based presentation. Students were then asked to take an online quiz that tested their knowledge of the new material, both immediately after learning the material and 2 wk later. Students who engaged in direct manipulation of the model scored higher on the assessment immediately after learning the material compared with the other two groups. However, there were no differences among the three groups when assessed after a 2-wk retention interval. Thus active learning techniques that involve direct interaction with the material can lead to learning benefits; however, how these techniques benefit long-term retention of the information is equivocal.

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.

Assessing Spatial Learning and Memory in Small Squamate Reptiles.

Clinical research has leveraged a variety of paradigms to assess cognitive decline, commonly targeting spatial learning and memory abilities. However, interest in the cognitive processes of nonmodel species, typically within an ecological context, has also become an emerging field of study. In particular, interest in the cognitive processes in reptiles is growing although experimental studies on reptilian cognition are sparse. The few reptilian studies that have experimentally tested for spatial learning and memory have used rodent paradigms modified for use in reptiles. However, ecologically important aspects of the physiology and behavior of this taxonomic group must be taken into account when testing for spatially based cognition. Here, we describe modifications of the dry land Barnes maze and associated testing protocol that can improve performance when probing for spatial learning and memory ability in small squamate reptiles. The described paradigm and procedures were successfully used with male side-blotched lizards (Uta stansburiana), demonstrating that spatial learning and memory can be assessed in this taxonomic group with an ecologically relevant apparatus and protocol.

Factors That Modulate Neurogenesis: A Top-Down Approach.

Although hippocampal neurogenesis in the adult brain has been conserved across the vertebrate lineage, laboratory studies have primarily examined this phenomenon in rodent models. This approach has been successful in elucidating important factors and mechanisms that can modulate rates of hippocampal neurogenesis, including hormones, environmental complexity, learning and memory, motor stimulation, and stress. However, recent studies have found that neurobiological research on neurogenesis in rodents may not easily translate to, or explain, neurogenesis patterns in nonrodent systems, particularly in species examined in the field. This review examines some of the evolutionary and ecological variables that may also modulate neurogenesis patterns. This 'top-down' and more naturalistic approach, which incorporates ecology and natural history, particularly of nonmodel species, may allow for a more comprehensive understanding of the functional significance of neurogenesis.

Environmental Change, the Stress Response, and Neurogenesis.

Previous to the 1980's, the prevailing neuroscience dogma held that no new neurons were produced in the brains of adult mammals. Now, we understand that the production of new neurons, or neurogenesis, is a common and plastic process in the adult brain. To date, however, researchers have not come to a unified understanding of the functional significance of neurogenesis. Several factors have been shown to modulate hippocampal neurogenesis including spatial learning, stress, and aspects of environmental change, but questions still remain. How do these modulating factors overlap? Which aspects of environmental change induce a stress response? Is there a relationship between hippocampal neurogenesis, the stress response, and environmental change? Can this relationship be altered when taking into consideration other factors such as perception and predictability of the environment? Finally, do results from neurobiological research on laboratory rodents translate to wild systems? This review attempts to address these questions and synthesize research from the fields of ecology, psychology, and behavioral neuroscience.

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.

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.

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.

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 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.

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.