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 avian hippocampus, homing in pigeons and the memory representation of large-scale space

The extraordinary navigational ability of homing pigeons providesa unique spatial cognitive system to investigate how the brainis able to represent past experiences as memory. In this paper,we first summarize a large body of lesion data in an attemptto characterize the role of the avian hippocampal formation(HF) in homing. What emerges from this analysis is the criticalimportance of HF for the learning of map-like, spatial representationsof environmental stimuli used for navigation. We then exploresome interesting properties of the homing pigeon HF, using fordiscussion the notion that the homing pigeon HF likely displayssome anatomical or physiological specialization(s), comparedto the laboratory rat, that account for its participation inhoming and the representation of large-scale, environmentalspace. Discussed are the internal connectivity among HF subdivisions,the occurrence of neurogenesis, the presence of rhythmic thetaactivity and the electrophysiological profile of HF neurons.Comparing the characteristics of the homing pigeon HF with thehippocampus of the laboratory rat, two opposing perspectivescan be supported. On the one hand, one could emphasize the subtledifferences in the properties of the homing pigeon HF as possibledeparture points for exploring how the homing pigeon HF maybe adapted for homing and the representation of large-scalespace. Alternatively, one could emphasize the similarities withthe rat hippocampus and suggest that, if homing pigeons representspace in a way different from rats, then the neural specializationsthat would account for the difference must lie outside HF. Onlyfuture research will determine which of these two perspectivesoffers a better approximation of the truth.     

Human memory: The hippocampus is the key

A recent study of brain-damaged patients with various degrees of amnesia provides compelling new evidence that the hippocampus plays a vital role in the laying down of new memories. Why existing memories are also affected by hippocampal damage is particularly puzzling.     

The hippocampus and memory: insights from spatial processing

The hippocampus appears to be crucial for long-term episodic memory, yet its precise role remains elusive. Electrophysiological studies in rodents offer a useful starting point for developing models of hippocampal processing in the spatial domain. Here we review one such model that points to an essential role for the hippocampus in the construction of mental images. We explain how this neural-level mechanistic account addresses some of the current controversies in the field, such as the role of the hippocampus in imagery and short-term memory, and discuss its broader implications for the neural bases of episodic memory.     

The hippocampus and memory: a comparative and ethological perspective

During the past year, considerable progress has been made in our understanding of the wide-ranging functions of the hippocampus. Highlights include the development of new tasks with which to assess spatial/topographic memory in humans and monkeys, novel tests of relational memory in rats, and episodic-like memory tasks in birds. In addition, novel theories of hippocampal function have been developed that are notable for their applicability to both humans and animal models.     

Neuronal networks and memory: role of the hippocampus

Learning and memory are related both to cognitive processes and to neurobiological mechanisms. The human pathology focused on the role of the hippocampus and animal experiments have analyzed its implications. The most usually admitted hypothesis is that memories are underlied by distributed specific neural networks defined through the strengthening of certain synapses, under the action of the flow of information during learning. The best candidate for this strengthening of the synapses is a change in synaptic plasticity similar to the artificial phenomenon of long-term potentiation. During memory processes, the hippocampus would play a particular role in information processing (analyzing novelty and significance of the information) and would allow the specification of the neural network, mainly in the cortical territories. We report data in olfactory learning in rats comforting these hypotheses. Considering neurochemistry of memory processes, specific synaptic changes and neuromodulatory processes must be distinguished. We report data about vasopressin illustrating both kinds of mechanisms in the hippocampus.     

The visual ecology of avian cone oil droplets

Summary Microspectrophotometric (msp) measurements were made of retinal oil droplets of 15 species of birds from 5 orders. The droplets were assigned to six categories on the basis of their cut-off wavelengths. Counts of oil droplets from the retinae of different species revealed large variations in the proportions of oil droplets of different categories. Cluster analysis was used to demonstrate relationships between 12 species of birds on the basis of their oil droplet complements. This analysis linked species in ways which were best explained by ecological factors and which only sometimes reflected phylogeny.Abbreviation msp microspectrophotometry     

The primate hippocampus: ontogeny, early insult and memory

Recent evidence suggests that in primates, as in rodents, the hippocampus shows a developmental continuum that affects memory abilities from infancy to adulthood. In primates relatively few hippocampal-dependent abilities (e.g. some aspects of recognition memory) are present in early infancy, whereas others (e.g. relational memory) begin to show adult-like characteristics around 2 years of age in monkeys and 5-7 years in humans. Profound and persistent memory loss resulting from insult to the hippocampus in infancy becomes evident in everyday behavior only later in childhood. This pattern of results suggests a maturational gradient within the medial temporal lobe memory system, with most abilities crucially dependent upon the hippocampus emerging in later stages of development, supporting a model of hierarchical organization of memory within the medial temporal lobe.     

Semantic memory and the human hippocampus

It has been unclear whether the hippocampus is uniquely important for episodic memory (memory for events that are specific to time and place) or whether the hippocampus is also important for learning and remembering facts (semantic memory). In two studies, we assessed the capacity for semantic memory in patients with bilateral damage thought to be restricted primarily to the hippocampal region who developed memory impairment at a known time. Since the onset of their memory impairment, the patients have acquired less factual knowledge than controls. The patients also exhibit temporally limited retrograde amnesia for factual information from the several years preceding the onset of memory impairment. Remote memory for factual knowledge (from 11-30 years before amnesia) is intact. The results show that the hippocampal region supports semantic memory as well as episodic memory and that its role in the acquisition and storage of semantic knowledge is time limited.     

Recognition memory and the human hippocampus

The capacity for declarative memory depends on the hippocampal region and adjacent cortex within the medial temporal lobe. One of the most widely studied examples of declarative memory is the capacity to recognize recently encountered material as familiar, but uncertainty remains about whether intact recognition memory depends on the hippocampal region itself and, if so, what the nature of the hippocampal contribution might be. Seven patients with bilateral damage thought to be limited primarily to the hippocampal region were impaired on three standard tests of recognition memory. In addition, the patients were impaired to a similar extent at Remembering and Knowing, measures of the two processes thought to support recognition performance: the ability to remember the learning episode (episodic recollection) and the capacity for judging items as familiar (familiarity).     

The human hippocampus and spatial and episodic memory

Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.     

Prevalence of avian influenza and host ecology

Waterfowl and shorebirds are common reservoirs of the low pathogenic subtypes of avian influenza (LPAI), which are easily transmitted to poultry and become highly pathogenic. As the risk of virus transmission depends on the prevalence of LPAI in host-reservoir systems, there is an urgent need for understanding how host ecology, life history and behaviour can affect virus prevalence in the wild. To test for the most important ecological correlates of LPAI virus prevalence at the interspecific level, we applied a comparative analysis by using quantitative data on 30 bird species. We controlled for similarity among species due to common descent, differences in study effort and for covariance among ecological variables. We found that LPAI prevalence is a species-specific attribute and is a consequence of virus susceptibility, as it was negatively associated with the relative size of the bursa of Fabricius, an estimate of juvenile immune function. Species that migrate long distances have elevated prevalence of LPAI independent of phylogeny and other confounding factors. There was also a positive interspecific relationship between the frequency of surface feeding and virus prevalence, but this was sensitive to phylogenetic relatedness of species. Feeding in marine habitats is apparently associated with lower virus prevalence, but the effect of water salinity is likely to be indirect and affected by phylogeny. Our results imply that virus transmission via surface waters and frequent intra- and interspecific contacts during long migration are the major risk factors of avian influenza in the wild. However, the link between exploitation of surface waters and LPAI prevalence appears to be weaker than previously thought. This is the first interspecific study that provides statistical evidence that host ecology, immunity and phylogeny have important consequence for virus prevalence.     

The rat brain hippocampus proteome

The hippocampus is crucial in memory storage and retrieval and plays an important role in stress response. In humans, the CA1 area of hippocampus is one of the first brain areas to display pathology in Alzheimer's disease. A comprehensive analysis of the hippocampus proteome has not been accomplished yet. We applied proteomics technologies to construct a two-dimensional database for rat brain hippocampus proteins. Hippocampus samples from eight months old animals were analyzed by two-dimensional electrophoresis and the proteins were identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. The database comprises 148 different gene products, which are in the majority enzymes, structural proteins and heat shock proteins. It also includes 39 neuron specific gene products. The database may be useful in animal model studies of neurological disorders.     

The role of hippocampus in long-term memory: dynamic system approach

Several attempts have been made to reconcile a number of concurrent theories on the role of the hippocampus in long-term memory functions. Those attempts fail to explain the basic effects of the theories from the same standpoint. This work is a critical review of the four major theories demonstrating (with the use of mathematical models of attention and memory) that only one of them is capable of reconciling them all by explaining the fundamental effects of each theory in a unified fashion without sacrificing their individual contributions. The key issue here is whether or not a memory trace is ever stored in the hippocampus itself, and there is no reconciliation unless the answer is in the negative.     

The hippocampus, spatial memory and food hoarding: a puzzle revisited

Behavioural ecology assumes that cognitive traits and their underlying neural substrates are shaped by natural selection in much the same way as morphological traits are, resulting in adaptation to the natural environment of the species concerned. Recently, however, the 'neuroecology' approach of attempting to gain insight into brain structure and function by testing predictions about variation in brain structure based on knowledge of the lifestyle of the animal has been criticized on the grounds that such an adaptationist view cannot provide insight into the underlying mechanisms. Furthermore, the criticism has focussed on attempts to use variation in demand for spatial memory and in hippocampal size as a basis for predicting variation in cognitive abilities. Here, we revisit this critique against the field of so-called 'neuroecology' and argue that using knowledge of the natural history of animals has lead to a better understanding of the interspecific variation in spatial abilities and hippocampal size, and to the generation of novel hypotheses and predictions.