Lara D. LaDage

Spatial memory and animal movement

Memory is critical to understanding animal movement but has proven challenging to study. Advances in animal tracking technology, theoretical movement models and cognitive sciences have facilitated research in each of these fields, but also created a need for synthetic examination of the linkages between memory and animal movement. Here, we draw together research from several disciplines to understand the relationship between animal memory and movement processes. First, we frame the problem in terms of the characteristics, costs and benefits of memory as outlined in psychology and neuroscience. Next, we provide an overview of the theories and conceptual frameworks that have emerged from behavioural ecology and animal cognition. Third, we turn to movement ecology and summarise recent, rapid developments in the types and quantities of available movement data, and in the statistical measures applicable to such data. Fourth, we discuss the advantages and interrelationships of diverse modelling approaches that have been used to explore the memory-movement interface. Finally, we outline key research challenges for the memory and movement communities, focusing on data needs and mathematical and computational challenges. We conclude with a roadmap for future work in this area, outlining axes along which focused research should yield rapid progress.

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.

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 individuals 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.

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 speciess 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.

Elevation-related differences in memory and the hippocampus in mountain chickadees, Poecile gambeli

Harsh environments may lead to increased demands on memory in animals that rely on memory for survival. We previously showed that winter severity is associated with non-experience-based differences in memory and the hippocampus over a large continental scale in food-caching black-capped chickadees, Poecile atricapillus. However, large climatic differences also occur along steep elevational gradients in montane environments over a small geographical scale. Here, we demonstrate for the first time that large differences in memory and the hippocampus exist over extremely short distances (10 km) along the elevation gradient. We found that food-caching mountain chickadees (P. gambeli) from the highest elevations in the Sierra Nevada Mountains had significantly better spatial memory associated with larger hippocampi, with almost twice the number of hippocampal neurons, than individuals only 600 m lower in elevation. We found similarly large differences in hippocampal neurogenesis rates as indicated by the total number of immature neurons. Our study therefore suggests that climate-related environmental differences can produce dramatic differences in memory and the hippocampus in animals within close proximity on small spatial scales and that currently observed trends in global climate may have significant effects on cognition and the brain.

Effects of Captivity and Memory-Based Experiences on the Hippocampus in Mountain Chickadees

The complexity of an animals 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.

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.

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.

Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies

Spatial abilities have been associated with many ecologically-relevant behaviors such as territoriality, mate choice, navigation and acquisition of food resources. Differential demands on spatial abilities in birds and mammals have been shown to affect the hippocampus, the region of the brain responsible for spatial processing. In some bird and mammal species, higher demands on spatial abilities are associated with larger hippocampal volumes. The medial and dorsal cortices are the putative reptilian homologues of the mammalian hippocampus, yet few studies have examined the relationship between these brain areas and differential spatial use strategies in reptiles. Further, many studies in birds and mammals compare hippocampal attributes between species that utilize space differently, potentially confounding species-specific effects with effects due to differential behaviors in spatial use. Here, we investigated the relationship between spatial use strategies and medial and dorsal cortical volumes in males of the side-blotched lizard (Uta stansburiana). In this species, males occur in three different morphs, each morph using different spatial niches: large territory holders, small territory holders and non-territory holders with home ranges smaller than the territories of small territory holders. We found that large territory holders had larger dorsal cortical volumes relative to the remainder of the telencephalon compared with non-territorial males, and small territory holders were intermediate. These results suggest that some aspect of holding a large territory may place demands on spatial abilities, which is reflected in a brain region thought partially responsible for spatial processing.