Seasonal hippocampal plasticity in food-storing birds

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

Septum volume and food-storing behavior are related in parids

The hippocampal formation (HF) of food-storing birds is larger than non-storing species, and the size of the HF in food-storing Black-Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non-storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food-storing Black-Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non-storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black-Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food-storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food-storing birds, may be specialized for some aspects of food-storing and spatial memory.     

Photoperiodic regulation of food storing and hippocampus volume in black-capped chickadees, Poecile atricapillus

In seasonal environments animals organize their behaviour around annual cycles of resource availability. Wild black-capped chickadees are most likely to hoard food in autumn. At this time of year chickadees are also reported to have a larger hippocampus, a brain area important for spatial memory. This study examined how photoperiodic condition affects these seasonal changes. Captive chickadees were exposed to one of three treatments. Photorefractory birds were held on long days (19:5 h light:dark) and had small gonads. Photosensitive birds were held on short days (LD 9:15 h) and also had small gonads. Photostimulated birds were switched from short to long days and quickly entered breeding condition with large gonads. Photosensitive birds (on short days) stored more seeds than photorefractory birds (on long days). Photostimulated birds stored seeds at a high rate when on short days, but reduced storing when transferred to long days. These results indicate that long days inhibit storing regardless of gonadal condition. There were no differences between groups in hippocampal volume, indicating that photoperiod can produce changes in food-storing behaviour without affecting hippocampal size. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Greater hippocampal neuronal recruitment in food-storing than in non-food-storing birds

Previous research has shown heightened recruitment of new neurons to the chickadee hippocampus in the fall. The present study was conducted to determine whether heightened fall recruitment is associated with the seasonal onset of food-storing by comparing neurogenesis in chickadees and a non-food-storing species, the house sparrow. Chickadees and house sparrows were captured in the wild in fall and spring and received multiple injections of the cell birth marker bromodeoxyuridine (BrdU). Birds were held in captivity and the level of hippocampal neuron recruitment was assessed after 6 weeks. Chickadees showed significantly more hippocampal neuronal recruitment than house sparrows. We found no seasonal differences in hippocampal neuronal recruitment in either species. In chickadees and in house sparrows, one-third of new cells labeled for BrdU also expressed the mature neuronal protein, NeuN. In a region adjacent to the hippocampus, the hyperpallium apicale, we observed no significant differences in neuronal recruitment between species or between seasons. Hippocampal volume and total neuron number both were greater in spring than in fall in chickadees, but no seasonal differences were observed in house sparrows. Enhanced neuronal recruitment in the hippocampus of food-storing chickadees suggests a degree of neurogenic specialization that may be associated with the spatial memory requirements of food-storing behavior.     

Septum volume and food‐storing behavior are related in parids

The hippocampal formation (HF) of food‐storing birds is larger than non‐storing species, and the size of the HF in food‐storing Black‐Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non‐storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food‐storing Black‐Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non‐storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black‐Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food‐storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food‐storing birds, may be specialized for some aspects of food‐storing and spatial memory. © 2002 Wiley Periodicals, Inc. J Neurobiol 51: 215–222, 2002     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

Inhibition of cell proliferation in black‐capped chickadees suggests a role for neurogenesis in spatial learning

Following development, the avian brain continues to produce neurons throughout adulthood, which functionally integrate throughout the telencephalon, including the hippocampus. In food‐storing birds like the black‐capped chickadee (Poecile atricapillus), new neurons incorporated into the hippocampus are hypothesized to play a role in spatial learning. Previous results on the relation between hippocampal neurogenesis and spatial learning, however, are correlational. In this study, we experimentally suppressed hippocampal neuronal recruitment and tested for subsequent effects on spatial learning in adult chickadees. After chickadees exhibited significant learning, we treated birds with daily injections of either saline or methylazoxymethanol (MAM), a toxin that suppresses cell proliferation in the brain and monitored subsequent spatial learning. MAM treatment significantly reduced cell proliferation around the lateral ventricles and neuronal recruitment in the hippocampus, measured using the cell birth marker bromodeoxyuridine. MAM‐treated birds performed significantly worse than controls on the spatial learning task 12 days following the initiation of MAM treatment, a time when new neurons would begin functionally integrating into the hippocampus. This difference in learning, however, was limited to a single trial. MAM treatment did not affect any measure of body condition, suggesting learning impairments were not a product of non‐specific adverse effects of MAM. This is the first evidence of a potential causal link between hippocampal neurogenesis and spatial learning in birds. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 74: 1002–1010, 2014     

Seasonal changes in hippocampus size and spatial behaviour in mammals and birds

Hippocampus is involved in processing of environmental spatial information, and its size is known to correlate positively with spatial abilities in mammals and birds. Comparisons between species suggest that amount of spatial information processed (the mean area of home range in particular) is related with hippocampus size. Do seasonal and age changes in hippocampus size correlate with seasonal dynamics of spatial behaviour during ontogenesis? The data obtained through observational and experimental studies confirm the possibility that hippocampus size may be subjected to adaptive modifications along with cyclic changes in spatial behavior. In course of seasonal dynamics, strong positive correlation was found between hippocampus mass, home range size, and mobility of small mammals. Recently, first facts demonstrating seasonal changes of hippocampus and spatial behaviour (in connection with food-storing and brood parasitism) were found in birds. A lot of facts obtained for different taxonomical groups shows parallel seasonal changes in spatial behaviour and morphology of brain region functionally related to such behaviour. Thus, in adult birds and mammals, not only behaviour but also brain structure is phenotypically flexible in response to seasonally changing environment. Morphophysiological mechanisms of hippocampus seasonal changes are also discussed.     

Cannabinoid inhibition improves memory in food-storing birds, but with a cost

Food-storing birds demonstrate remarkable memory ability in recalling the locations of thousands of hidden food caches. Although this behaviour requires the hippocampus, its synaptic mechanisms are not understood. Here we show the effects of cannabinoid receptor (CB1-R) blockade on spatial memory in food-storing black-capped chickadees (Poecile atricapilla). Intra-hippocampal infusions of the CB1-R antagonist SR141716A enhanced long-term memory for the location of a hidden food reward, measured 72 h after encoding. However, when the reward location changed during the retention interval, birds that had received SR141716A during initial learning showed impairments in recalling the most recent reward location. Thus, blocking CB1-R activity may lead to more robust, long-lasting memories, but these memories may be a source of proactive interference. The relationship between trace strength and interference may be important in understanding neural mechanisms of hippocampal function in general, as well as understanding the enhanced memory of food-storing birds.     

Seasonal variation in pectoralis muscle and heart myostatin and tolloid-like proteinases in small birds: a regulatory role for seasonal phenotypic flexibility?

Seasonally variable environments produce seasonal phenotypes in small birds such that winter birds have higher thermogenic capacities and pectoralis and heart masses. One potential regulator of these seasonal phenotypes is myostatin, a muscle growth inhibitor, which may be downregulated under conditions promoting increased energy demand. We examined summer-to-winter variation in skeletal muscle and heart masses and used qPCR and Western blots to measure levels of myostatin and its metalloproteinase activators TLL-1 and TLL-2 for two small temperate-zone resident birds, American goldfinches (Spinus tristis) and black-capped chickadees (Poecile atricapillus). Winter pectoralis and heart masses were significantly greater than in summer for American goldfinches. Neither myostatin expression nor protein levels differed significantly between seasons for goldfinch pectoralis. However, myostatin levels in goldfinch heart were significantly greater in summer than in winter, although heart myostatin expression was seasonally stable. In addition, expression of both metalloproteinase activators was greater in summer than in winter goldfinches for both pectoralis and heart, significantly so except for heart TLL-2 (P = 0.083). Black-capped chickadees showed no significant seasonal variation in muscle or heart masses. Seasonal patterns of pectoralis and heart expression and/or protein levels for myostatin and its metalloproteinase activators in chickadees showed no consistent seasonal trends, which may help explain the absence of significant seasonal variation in muscle or heart masses for chickadees in this study. These data are partially consistent with a regulatory role for myostatin, and especially myostatin processing capacity, in mediating seasonal metabolic phenotypes of small birds.     

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

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

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

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

Prolonged moderate elevation of corticosterone does not affect hippocampal anatomy or cell proliferation rates in mountain chickadees (Poecile gambeli)

Chronic stress and corresponding chronic elevations of glucocorticoid hormones have been widely assumed to have deleterious effects on brain anatomy and functions such as learning and memory. In particular, it has been suggested that chronic elevations of glucocorticoid hormones result in death of hippocampal neurons and in reduced rates of hippocampal neurogenesis. It is not clear, however, if any increase in glucocorticoid levels has negative effects on hippocampal anatomy as many animals regularly maintain moderately elevated levels of glucocrticoids over long periods of time under natural energetically demanding conditions. We used unbiased stereological methods to investigate whether mountain chickadees (Poecile gambeli) implanted for 49 days with continuous time-release corticosterone pellets, designed to approximately double the baseline corticosterone levels, differed from placebo-implanted chickadees in their hippocampal anatomy and cell proliferation rates. We found no significant differences between corticosterone and placebo-implanted birds in either telencephalon volume, volume of the hippocampal formation, or the total number of hippocampal neurons. Cell proliferation rates, measured as the total number of BrdU-labeled cells in the ventricular zone adjacent either to the hippocampus or to the mesopallium, were also not significantly different between corticosterone and placebo-implanted chickadees. Our results suggest that prolonged moderate elevation of corticosterone might not provide the suggested deleterious effects on hippocampal anatomy and neurogenesis in food-caching birds and, as we have shown previously, it actually enhances spatial memory.     

Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees

It is well established that spatial memory is dependent on the hippocampus in both mammals and birds. As memory capacity can fluctuate on a temporal basis, it is important to understand the mechanisms mediating such changes. It is known that early memory-dependent experiences in young animals result in hippocampal enlargement and in increased neurogenesis, including cell proliferation and neuron survival. It is less clear, however, whether temporal changes in spatial memory are also associated with changes in hippocampal anatomy and cell proliferation in fully grown and experienced adult animals. In a previous study, we experimentally demonstrated that socially subordinate mountain chickadees (Poecile gambeli) showed inferior spatial memory performance compared to their dominant group mates, in the absence of significant differences in baseline corticosterone levels. Here we investigated whether these differences in memory between dominant and subordinate birds were associated with changes in the hippocampus. Following memory tests, chickadees were injected with 5-bromo-2'-deoxyuridine to label dividing cells and sacrificed 2 days after the injections. We found no significant differences in volume or the total number of neurons in the hippocampal formation between dominant and subordinate chickadees, but subordinate birds had significantly lower cell proliferation rates in the ventricular zone adjacent to both the hippocampus and mesopallium compared to the dominants. Individuals, which performed better on spatial memory tests tended to have higher levels of cell proliferation. These results suggest that social status can affect cell proliferation rates in the ventricular zone and support the hypothesis that neurogenesis might be involved in memory function in adult animals.     

Dominance‐related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees

It is well established that spatial memory is dependent on the hippocampus in both mammals and birds. As memory capacity can fluctuate on a temporal basis, it is important to understand the mechanisms mediating such changes. It is known that early memory‐dependent experiences in young animals result in hippocampal enlargement and in increased neurogenesis, including cell proliferation and neuron survival. It is less clear, however, whether temporal changes in spatial memory are also associated with changes in hippocampal anatomy and cell proliferation in fully grown and experienced adult animals. In a previous study, we experimentally demonstrated that socially subordinate mountain chickadees (Poecile gambeli) showed inferior spatial memory performance compared to their dominant group mates, in the absence of significant differences in baseline corticosterone levels. Here we investigated whether these differences in memory between dominant and subordinate birds were associated with changes in the hippocampus. Following memory tests, chickadees were injected with 5‐bromo‐2′‐deoxyuridine to label dividing cells and sacrificed 2 days after the injections. We found no significant differences in volume or the total number of neurons in the hippocampal formation between dominant and subordinate chickadees, but subordinate birds had significantly lower cell proliferation rates in the ventricular zone adjacent to both the hippocampus and mesopallium compared to the dominants. Individuals, which performed better on spatial memory tests tended to have higher levels of cell proliferation. These results suggest that social status can affect cell proliferation rates in the ventricular zone and support the hypothesis that neurogenesis might be involved in memory function in adult animals. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2005     

Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions

Black-capped chickadees have a rich vocal repertoire including learned calls and the learned fee-bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee-bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal-control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal-control regions to produce learned calls year-round.     

Captivity reduces hippocampal volume but not survival of new cells in a food‐storing bird

In many naturalistic studies of the hippocampus wild animals are held in captivity. To test if captivity itself affects hippocampal integrity, adult black‐capped chickadees (Poecile atricapilla) were caught in the fall, injected with bromodeoxyuridine to mark neurogenesis, and alternately released to the wild or held in captivity. The wild birds were recaptured after 4–6 weeks and perfused simultaneously with their captive counterparts. The hippocampus of captive birds was 23% smaller than wild birds, with no hemispheric differences in volume within groups. Between groups there was no statistically significant difference in the size of the telencephalon, or in the number and density of surviving new cells. Proximate causes of the reduced hippocampal volume could include stress, lack of exercise, diminished social interaction, or limited caching opportunity—a hippocampal‐dependent activity. The results suggest the avian hippocampus—a structure essential for rapid, complex relational and spatial learning—is both plastic and sensitive, much as in mammals, including humans. © 2009 Wiley Periodicals, Inc. Develop Neurobiol, 2009     

Annual cycle of the black‐capped chickadee: Seasonality of singing rates and vocal‐control brain regions

Black‐capped chickadees have a rich vocal repertoire including learned calls and the learned fee‐bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee‐bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal‐control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal‐control regions to produce learned calls year‐round. © 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

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

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