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.     

Food-storing birds: adaptive specialization in brain and behaviour?

Among the passerine birds, species that store food have an enlarged hippocampal region (dorso-medial cortex), relative to brain and body size, when compared with the non-storers. The volume of one of the major afferent-efferent pathways (the septo-hippocampal pathway) is also greater in food storing species. This specialization of brain structure is discussed in relation to behavioural studies in which the spatial memory of storing and non-storing species has been compared.     

Long-term tryptophan administration enhances cognitive performance and increases 5HT metabolism in the hippocampus of female rats

Summary. It has been shown in various studies that increase in serotonergic neurotransmission is associated with increased memory consolidation whereas low brain 5HT impairs memory performance. In the first phase of our study we found that tryptophan (TRP) administration for 6 weeks increased plasma TRP and whole brain TRP, 5HT and 5HIAA levels. Many brain regions are involved in the learning process but particularly the hippocampus is known to have key role in learning and memory. The present study was therefore designed to investigate the effects of TRP loading particularly on hippocampal 5HT metabolism and cognitive performance in rats. TRP-treated rats demonstrated spatial enhancement as evidenced by a significant decrease in time to find the hidden food reward in radial arm maze test (RAM). The important finding of the present study was the greater increase in the 5HT metabolism in hippocampus than in any other brain region of the TRP-treated rats. This increased 5HT metabolism in the hippocampus emphasizes the involvement of this region in memory process.     

Does Sleep Play a Role in Memory Consolidation? A Comparative Test

Sleep is a pervasive characteristic of mammalian species, yet its purpose remains obscure. It is often proposed that ‘sleep is for the brain’, a view that is supported by experimental studies showing that sleep improves cognitive processes such as memory consolidation. Some comparative studies have also reported that mammalian sleep durations are higher among more encephalized species. However, no study has assessed the relationship between sleep and the brain structures that are implicated in specific cognitive processes across species. The hippocampus, neocortex and amygdala are important for memory consolidation and learning and are also in a highly actived state during sleep. We therefore investigated the evolutionary relationship between mammalian sleep and the size of these brain structures using phylogenetic comparative methods. We found that evolutionary increases in the size of the amygdala are associated with corresponding increases in NREM sleep durations. These results are consistent with the hypothesis that NREM sleep is functionally linked with specializations of the amygdala, including perhaps memory processing.     

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.     

Is hippocampal volume affected by specialization for food hoarding in birds?

The hypothesis that spatial-memory specialization affects the size of the hippocampus has become widely accepted among scientists. The hypothesis comes from studies on birds primarily in two families, the Paridae (tits, titmice and chickadees) and the Corvidae (crows, nutcrackers, jays, etc.). Many species in these families store food and rely on spatial memory to relocate the cached items. The hippocampus is a brain structure that is thought to be important for memory. Several studies report that hoarding species in these families possess larger hippocampi than non-hoarding relatives, and that species classified as large-scale hoarders have larger hippocampi than less specialized hoarders. We have investigated the largest dataset on hippocampus size and food-hoarding behaviour in these families so far but did not find a significant correlation between food-hoarding specialization and hippocampal volume. The occurrence of such an effect in earlier studies may depend on differences in the estimation of hippocampal volumes or difficulties in categorizing the degree of specialization for hoarding or both. To control for discrepancies in measurement methods we made our own estimates of hippocampal volumes in 16 individuals of four species that have been included in previous studies. Our estimates agreed closely with previous ones, suggesting that measurement methods are sufficiently consistent. Instead, the main reasons that previous studies have found an effect where we did not are difficulties in assessing the degree of hoarding specialization and the fact that smaller subsets of species were compared than in our study. Our results show that a correlation between food-hoarding specialization and hippocampal volume cannot be claimed on the basis of present data in these families.     

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.     

The evolution of hippocampus volume and brain size in relation to food hoarding in birds

Food‐hoarding birds frequently use spatial memory to relocate their caches, thus they may evolve a larger hippocampus in their brain than non‐hoarder species. However, previous studies testing for such interspecific relationships provided conflicting results. In addition, food hoarding may be a cognitively complex task involving elaboration of a variety of brain regions, even outside of the hippocampus. Hence, specialization to food hoarding may also result in the enlargement of the overall brain. In a phylogenetic analysis of distantly related birds, we studied the interspecific association between food hoarding and the size of different brain regions, each reflecting different resolutions. After adjusting for allometric effects, the relative volume of the hippocampus and the relative size of the entire brain were each positively related to the degree of food‐hoarding specialization, even after controlling for migration and brood parasitism. We also found some significant evidence for the relative volume of the telencephalon being associated with food hoarding, but this relationship was dependent on the approach we used. Hence, neural adaptation to food hoarding may favour the evolution of different brain structures.     

Common molecular mechanisms in explicit and implicit memory

Cellular and molecular studies of both implicit and explicit memory suggest that experience-dependent modulation of synaptic strength and structure is a fundamental mechanism by which these memories are encoded and stored within the brain. In this review, we focus on recent advances in our understanding of two types of memory storage: (i) sensitization in Aplysia, a simple form of implicit memory, and (ii) formation of explicit spatial memories in the mouse hippocampus. These two processes share common molecular mechanisms that have been highly conserved through evolution.     

Intra CA1 insulin microinjection improves memory consolidation and retrieval

Although the brain was considered as an insulin-insensitive organ, recent studies have shown that insulin receptors exist in the brain and insulin modulates some of the brain tasks. Insulin and its receptor are found in specific areas of CNS with a variety of region-specific functions different from its direct glucose regulation in the periphery. The hippocampus and cerebral cortex distributed insulin/insulin receptor has been shown to be involved in brain cognitive functions. The improving effect of insulin on spatial memory acquisition has been shown. In the present study, the effect of insulin microinjection into the CA1 region of rat hippocampus on spatial memory consolidation and retrieval has been investigated. Insulin in 12 MU (but not in 0.5 and 6 MU) improved both memory retrieval and consolidation.     

The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison

It has been hypothesized that memory-demanding ecological conditions might result in enhanced memory and an enlarged hippocampus, an area of the brain involved in memory processing, either via extensive memory experience or through evolutionary changes. Avian migration appears to represent one of such memory-demanding ecological conditions. We compared two subspecies of the white-crowned sparrow: migratory Zonotrichia leucophrys gambelii and non-migratory Z. l. nuttalli. Compared to non-migratory Z. l. nuttalli, migratory Z. l. gambelii showed better memory performance on spatial one-trial associative learning tasks and had more hippocampal neurons. Migratory subspecies also had larger hippocampi relative to the remainder of the telencephalon but not relative to body mass. In adults, the differences between migratory and non-migratory sparrows were especially pronounced in the right hippocampus. Juvenile migratory Z. l. gambelii had relatively larger hippocampal volume compared to juvenile non-migratory Z. l. nuttalli. Adult migratory Z. l. gambelii had more neurons in their right hippocampus compared to juveniles but such differences were not found in non-migratory Z. l. nuttalli. Our results suggest that migratory behaviour might be related to enhanced spatial memory and an enlarged hippocampus with more neurons, and that differences in the hippocampus between migratory and non-migratory sparrows might be experience-dependent. Furthermore, for the first time our results suggest that the right hippocampus, which encodes global spatial information, might be involved in migratory behaviour.     

Neuroecology and diet selection in phyllostomid bats

For many birds and mammals relative brain and hippocampus volume are positively related to enhanced behavioral flexibility and spatial memory. I tested for correlations between species-specific diet selection and relative brain and hippocampus volumes in the New World leaf-nosed bats (Phyllostomidae). To this end, I classified each of 53 species from this ecologically diverse family as one of the following: (i) predatory, (ii) omnivorous, (iii) frugivorous, or (iv) nectivorous. Species-level analyses and the comparative method (i.e. phylogenetically independent contrasts) revealed that relative hippocampus volume was greater in predatory species than in frugivorous and nectivorous species and that relative brain size was greater in frugivorous species than in predatory species. As previously reported, specialized frugivory appears to be associated with increased relative brain volume suggesting these two traits evolve together. I suggest some plausible functional explanations for variation in hippocampus volume in light of our current understanding of the acquisition of spatial information and its use by echolocating bats.     

The importance of neural aromatization in the acquisition,recall, and integration of song and spatial memories in passerines

This article is part of a Special Issue “Estradiol and cognition”.In addition to their well-studied and crucial effects on brain development and aging, an increasing number of investigations across vertebrate species indicate that estrogens like 17β-estradiol (E₂) have pronounced and rapid effects on cognitive function. The incidence and regulation of the E₂-synthesizing enzyme aromatase at the synapse in regions of the brain responsible for learning, memory, social communication and other complex cognitive processes suggest that local E₂ production and action affect the acute and chronic activity of individual neurons and circuits. Songbirds in particular are excellent models for the study of this “synaptocrine” hormone provision given that aromatase is abundantly expressed in neuronal soma, dendrites, and at the synapse across many brain regions in both sexes. Additionally, songbirds readily acquire and recall memories in laboratory settings, and their stereotyped behaviors may be manipulated and measured with relative ease. This leads to a rather unparalleled advantage in the use of these animals in studies of the role of neural aromatization in cognition. In this review we describe the results of a number of experiments in songbird species with a focus on the influence of synaptic E₂ provision on two cognitive processes: auditory discrimination reliant on the caudomedial nidopallium (NCM), a telencephalic region likely homologous to the auditory cortex in mammals, and spatial memory dependent on the hippocampus. Data from these studies are providing evidence that the local and acute provision of E₂ modulates the hormonal, electrical, and cognitive outputs of the vertebrate brain and aids in memory acquisition, retention, and perhaps the confluence of memory systems.     

Mechanisms of cache retrieval in long-term hoarding birds

Food hoarding and memory have primarily been studied in two bird families, the Corvidae (crows, jays, nutcrackers, etc.) and the Paridae (tits, titmice and chickadees). In both families there are species that hoard large quantities of seeds and nuts in the autumn and depend on these stores during the winter. Caches are concealed or highly inconspicuous and the most efficient way to retrieve them is to remember the exact locations. However, a long-term memory for a large number of caches may be physiologically expensive, and especially after long retention intervals, an alternative strategy could be to retrieve caches by cheaper but less efficient methods. Very few studies have been designed to investigate the decay of the memory in birds, but both field observations and experiments point in the same direction: although long-term hoarding corvids seem to possess an accurate long-term memory, long-term hoarding parids do not appear to. I discuss possible reasons for this and suggest that differences between the families in their degree of dependence on stored food or/and size-related limitations of brain capacity may be important.     

Defining structural homology between the mammalian and avian hippocampus through conserved gene expression patterns observed in the chick embryo

The mammalian hippocampus, a center of neurogenesis in the adult brain, is involved in critical functions such as learning and memory processing. Although there is an overall functional conservation between birds and mammals in the hippocampal region of the brain, there are several morphological differences. A few different models have been proposed for identifying regional and structural homology between the avian and mammalian hippocampus however a consensus is yet to be reached. In this study we have systematically and comprehensively characterized the developing chicken hippocampus at the molecular level. We have identified the time window of neurogenesis and apoptosis during hippocampal development as well as the likely origin and migration path of neurons of the ventral v-shaped region of chick hippocampus. In addition to this we have identified several genes with expression patterns that are conserved between the hippocampus of chicken and mice. Our study provides molecular data that partially supports one of the models reported in literature for structural homology between the avian and mammalian hippocampus. Functional characterization of the genes found in this study to be specifically expressed in the developing chicken hippocampus is likely to provide valuable information on the mechanisms regulating hippocampus development of birds and perhaps could be extrapolated to mammalian hippocampus development as well.     

A Network Convergence Zone in the Hippocampus

The hippocampal formation is a key structure for memory function in the brain. The functional anatomy of the brain suggests that the hippocampus may be a convergence zone, as it receives polysensory input from distributed association areas throughout the neocortex. However, recent quantitative graph-theoretic analyses of the static large-scale connectome have failed to demonstrate the centrality of the hippocampus; in the context of the whole brain, the hippocampus is not among the most connected or reachable nodes. Here we show that when communication dynamics are taken into account, the hippocampus is a key hub in the connectome. Using a novel computational model, we demonstrate that large-scale brain network topology is organized to funnel and concentrate information flow in the hippocampus, supporting the long-standing hypothesis that this region acts as a critical convergence zone. Our results indicate that the functional capacity of the hippocampus is shaped by its embedding in the large-scale connectome.     

New circuits for old memories: the role of the neocortex in consolidation

Studies of learning and memory have provided a great deal of evidence implicating hippocampal mechanisms in the initial storage of facts and events. However, until recently, there were few hints as to how and where this information was permanently stored. A recent series of rodent molecular and cellular cognition studies provide compelling evidence for the involvement of specific neocortical regions in the storage of information initially processed in the hippocampus. Areas of the prefrontal cortex, including the anterior cingulate and prelimbic cortices, and the temporal cortex show robust increases in activity specifically following remote memory retrieval. Importantly, damage to or inactivation of these areas produces selective remote memory deficits. Additionally, transgenic studies provide glimpses into the molecular and cellular mechanisms underlying cortical memory consolidation. The studies reviewed here represent the first exciting steps toward the understanding of the molecular, cellular, and systems mechanisms of how the brain stores our oldest and perhaps most defining memories.     

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.     

Memory beyond the synapse

Based on studies of the molecular and cellular cascades that occur during memory consolidation for a one-trial passive-avoidance learning task in the young chick, I review the evidence that memory is encoded in permanent changes in synaptic connectivity ina specific brain region, the Hebb hypothesis. I conclude that despite the fact that such a cascade occurs, culminating in the synthesis of cell-adhesion molecules that are involved in synaptic remodelling, synaptic events are not in themselves sufficient to account for the phenomena of memory. Both whole brain (neuromodulator) and whole body (hormonal) processes are engaged.Memories are labile, disarticulated and stored in a distributed manner; how the mind/brain recreates coherent memories from this pattern is a mystery.     

Rats answer an unexpected question after incidental encoding

A fundamental aspect of episodic memory is that retrieval of information can occur when encoding is incidental and memory assessment is unexpected. These features are difficult to model in animals because behavioral training likely gives rise to well-learned expectations about the sequence of events. Thus, the possibility remains that animals may solve an episodic memory test by using well-learned semantic rules without remembering the episode at memory assessment. Here we show that rats can answer an unexpected question after incidental encoding in a hippocampal-dependent manner, consistent with the use of episodic memory. Rats were initially trained to report about a recent event (food versus no food) and separately searched for food where there was no expectation of being asked about the presence of food. To test episodic memory, we gave rats the opportunity to incidentally encode the presence or absence of food and unexpectedly asked them to report about the recent event. Temporary inactivation of the CA3 region of the hippocampus with bilateral infusions of lidocaine selectively eliminated the ability of rats to answer the unexpected, but not the expected, question. Our studies suggest that rats remember an earlier episode after incidental encoding based upon hippocampal-dependent episodic memory.