The seasonal hippocampus of food-storing birds

Food storing is seasonal in birds like chickadees, nuthatches and jays, occurring at high levels in fall and winter and low levels in spring and summer. Memory for cache sites is hippocampus dependent in chickadees and both the recruitment of new neurons into the hippocampus and the total size of the hippocampus change seasonally. Unlike seasonal change in the vocal control nuclei of songbirds, however, change in the hippocampus appears not to be controlled by photoperiod. The annual timing of hippocampal neuronal recruitment and change in hippocampal size is quite variable, reaching maximum levels at different times of year in different studies. The amount of food-storing activity by chickadees is known to be influenced by flock dominance structure, energy balance, food availability, and other seasonally varying factors. The variable timing of seasonal change in the hippocampus may indicate that the hippocampus of food-storing birds changes annually in response to change in the intensity of food storing behaviour itself.     

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.     

A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects

We conducted a comparative study of the peripheral auditory system in six avian species (downy woodpeckers, Carolina chickadees, tufted titmice, white-breasted nuthatches, house sparrows, and European starlings). These species differ in the complexity and frequency characteristics of their vocal repertoires. Physiological measures of hearing were collected on anesthetized birds using the auditory brainstem response to broadband click stimuli. If auditory brainstem response patterns are phylogenetically conserved, we predicted woodpeckers, sparrows, and starlings to be outliers relative to the other species, because woodpeckers are in a different Order (Piciformes) and, within the Order Passeriformes, sparrows and starlings are in different Superfamilies than the nuthatches, chickadees, and titmice. However, nuthatches and woodpeckers have the simplest vocal repertoires at the lowest frequencies of these six species. If auditory brainstem responses correlate with vocal complexity, therefore, we would predict nuthatches and woodpeckers to be outliers relative to the other four species. Our results indicate that auditory brainstem responses measures in the spring broadly correlated with both vocal complexity and, in some cases, phylogeny. However, these auditory brainstem response patterns shift from spring to winter due to species-specific seasonal changes. These seasonal changes suggest plasticity at the auditory periphery in adult birds.     

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.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning.

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open-ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age-limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [3H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open-ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open‐ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age‐limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [³H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open‐ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive. © 1999 John Wiley & Sons, Inc. J Neurobiol 40: 316–326, 1999     

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     

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     

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.     

Songbirds tradeoff auditory frequency resolution and temporal resolution

Physical tradeoffs may in some cases constrain the evolution of sensory systems. The peripheral auditory system, for example, performs a spectral decomposition of sound that should result in a tradeoff between frequency resolution and temporal resolution. We assessed temporal resolution in three songbird species using auditory brainstem responses to paired click stimuli. Temporal resolution was greater in house sparrows (Passer domesticus) than Carolina chickadees (Poecile carolinensis) and white-breasted nuthatches (Sitta carolinensis), as predicted based on previous observations of broader auditory filters (lower frequency resolution) in house sparrows. Furthermore, within chickadees, individuals with broader auditory filters had greater temporal resolution. In contrast to predictions however, temporal resolution was similar between chickadees and nuthatches despite broader auditory filters in chickadees. These results and the results of a model simulation exploring the effect of broadened auditory filter bandwidth on temporal resolution in the auditory periphery strongly suggest that frequency resolution constrains temporal resolution in songbirds. Furthermore, our results suggest that songbirds have greater temporal resolution than some mammals, in agreement with recent behavioral studies. Species differences in temporal resolution may reflect adaptations for efficient processing of species-specific vocalizations, while individual differences within species may reflect experience-based developmental plasticity or hormonal effects.     

Species‐specific injury‐induced cell proliferation in the hippocampus and subventricular zone of food‐storing and nonstoring wild birds

Cells are continuously born and incorporated into the adult hippocampus (HP). Adult neurogenesis might act to increase the total number of cells or replace dead cells. Thus, neurogenesis might be a primary factor in augmenting, maintaining, or even recovering functions. In zebra finches, HP injury increases cell proliferation in the HP and stem cell rich subventricular zone (SVZ). It is unknown what effect injury has on a species dependent upon the HP for survival in the wild. In food‐storing birds, recovery of caches is seasonal, necessary for survival, dependent upon the HP and is concomitant with a peak in HP neurogenesis. During the fall, food‐storing black‐capped chickadees (BCCs) and nonstoring dark‐eyed juncos (DEJs) were captured and given a unilateral penetrating lesion to the HP one day later. On day 3, birds were injected with the mitotic marker 5‐bromo‐2′‐deoxyuridine (BrdU) and perfused on day 10. If unlesioned, more BrdU‐labeled cells were observed in the HP and SVZ of BCCs compared to DEJs, indicating higher innate cell proliferation or incorporation in BCCs. If lesioned, BrdU‐labeled cells increased in the injured HP of both species; however, lesions caused larger increases in DEJs. DEJs also showed increases in BrdU‐labeled cells in the SVZ and contralateral HP. BCCs showed no such increases on day 10. Thus, during the fall food‐storing season, storers showed suppressed injury‐induced cell proliferation and/or reduced survival rates of these new cells compared to nonstorers. These species differences may provide a useful model for isolating factors involved in cellular responses following injury. © 2009 Wiley Periodicals, Inc. Develop Neurobiol, 2010     

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     

Seasonal metabolic acclimatization in mountain chickadees and juniper titmice

Mountain chickadees and juniper titmice from northern Utah were examined to determine metabolic and body-composition characteristics associated with seasonal acclimatization. These species use behavioral adaptations and nocturnal hypothermia, which reduce energetic costs. These adjustments could reduce the need for extensive metabolic adjustments typically found in small passerines that overwinter in cold regions. In addition, these species live at higher altitudes, which may also decrease metabolic acclimatization found in birds. Winter birds tolerated colder test temperatures than summer birds. This improved cold tolerance was associated with an increase in maximal thermogenic capacity or summit metabolism (M(sum)). Winter M(sum) exceeded summer M(sum) by 26.1% in chickadees and 16.2% in titmice. Basal metabolic rates (BMR) were also significantly higher in winter birds compared with summer birds. Pectoralis wet muscle mass increased 33.3% in chickadees and 24.1% in titmice in winter and paralleled the increased M(sum) and BMR. Dry mass of contour plumage increased in winter for both species and was associated with decreased thermal conductance in winter chickadees compared to summer chickadees. Chickadees and titmice show metabolic acclimatization similar to other temperate species.     

Phenotypic flexibility in passerine birds: Seasonal variation of aerobic enzyme activities in skeletal muscle

Improved winter cold tolerance is widespread among small passerines resident in cold climates and is generally associated with elevated summit metabolic rate (M_sum=maximum thermoregulatory metabolic rate) and improved shivering endurance with increased reliance on lipids as fuel. Elevated M_sum and improved cold tolerance may result from greater metabolic intensity, due to mass-specific increase in oxidative enzyme capacity, or increase in the masses of thermogenic tissues. To examine the mechanisms underlying winter increases in M_sum, we investigated seasonal changes in mass-specific and total activities of the key aerobic enzymes citrate synthase (CS) and β-hydroxyacyl CoA-dehydrogenase (HOAD) in pectoralis, supracoracoideus and mixed leg muscles of three resident passerine species, black-capped chickadee (Poecile atricapillus), house sparrow (Passer domesticus), and white-breasted nuthatch (Sitta carolinensis). Activities of CS were generally higher in winter than in summer muscles for chickadees and house sparrows, but not nuthatches. Mass-specific HOAD activity was significantly elevated in winter relative to summer in all muscles for chickadees, but did not vary significantly with season for sparrows or nuthatches, except for sparrow leg muscle. These results suggest that modulation of substrate flux and cellular aerobic capacity in muscle contribute to seasonal metabolic flexibility in some species and tissues, but such changes play varying roles among small passerines resident in cold climates.     

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.     

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.     

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.     

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.     

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