Elsevier

Neuropharmacology

Volume 37, Issues 4–5, 5 April 1998, Pages 441-452
Neuropharmacology

Review
Memory and the hippocampus in food-storing birds: a comparative approach

https://doi.org/10.1016/S0028-3908(98)00037-9Get rights and content

Abstract

Comparative studies provide a unique source of evidence for the role of the hippocampus in learning and memory. Within birds and mammals, the hippocampal volume of scatter-hoarding species that cache food in many different locations is enlarged, relative to the remainder of the telencephalon, when compared with than that of species which cache food in one larder, or do not cache at all. Do food-storing species show enhanced memory function in association with the volumetric enlargement of the hippocampus? Comparative studies within the parids (titmice and chickadees) and corvids (jays, nutcrackers and magpies), two families of birds which show natural variation in food-storing behavior, suggest that there may be two kinds of memory specialization associated with scatter-hoarding. First, in terms of spatial memory, several scatter-hoarding species have a more accurate and enduring spatial memory, and a preference to rely more heavily upon spatial cues, than that of closely related species which store less food, or none at all. Second, some scatter-hoarding parids and corvids are also more resistant to memory interference. While the most critical component about a cache site may be its spatial location, there is mounting evidence that food-storing birds remember additional information about the contents and status of cache sites. What is the underlying neural mechanism by which the hippocampus learns and remembers cache sites? The current mammalian dogma is that the neural mechanisms of learning and memory are achieved primarily by variations in synaptic number and efficacy. Recent work on the concomitant development of food-storing, memory and the avian hippocampus illustrates that the avian hippocampus may swell or shrivel by as much as 30% in response to presence or absence of food-storing experience. Memory for food caches triggers a dramatic increase in the total number of number of neurons within the avian hippocampus by altering the rate at which these cells are born and die.

Introduction

The most challenging question for contemporary neuroscience is to determine the mechanisms by which the brain encodes, stores and processes information. The relationship between memory and the hippocampus has fascinated neuroscientists ever since the discovery that HM and other patients with hippocampal damage suffer severe memory loss and learning deficits (Scoville and Milner, 1957, Milner et al., 1968). The general consensus is that this brain region plays a role in the acquisition and consolidation of long term memories (LTM) as opposed to being the site of memory storage (e.g. Squire, 1992). While the hippocampus has been implicated in several types of learning and memory, contemporary theories suggest that the hippocampus may have a general function in minimizing memory interference (Shapiro and Olton, 1994) and in forming complex configural associations between various environmental stimuli, associations which need not necessarily be spatial although they frequently are (e.g. Sutherland and Rudy, 1989, Squire, 1992, Eichenbaum et al., 1992, Eichenbaum, 1996).

Experiments conducted using animal models suggest that spatial memory tests provide one of the best behavioral markers of hippocampal function (O’Keefe and Nadel, 1978, Nadel, 1991). One explanation for this is that in creating a spatial map of the test environment, an animal typically forms configural associations between stimuli. Studies of the effects of hippocampal lesions on spatial memory performance in the Morris water maze (Morris, 1981, Morris et al., 1982), and electrophysiological recordings of ‘place cells’ in the hippocampus which fire only when the animal is in a certain position in the environment (O’Keefe 1979; see McNaughton et al., 1996for a recent review, but see Golob and Taube, 1997), lend considerable support to the hypothesis that the hippocampus plays an important role in spatial memory processing in animals.

Many of these animal experiments have been carried out using nocturnal species of rodents which have poor visual acuity but exceptional olfactory capabilities. To test spatial memory capabilities, typically the rodent is placed in a tank of cloudy water (e.g. Morris, 1981) or in a radial arm maze (e.g. Olton and Samuelson, 1976), where they are required to use visuo-spatial cues to perform the task. Visual cues may be more appropriate than olfactory cues for accurately predicting the spatial location of the reward, be it a platform or a food source, and this difference in cue reliability may explain why even nocturnal animals may prefer visual cues over olfactory ones when tested in certain laboratory paradigms (Lavenex and Schenk, 1995). However, considerable future progress may be made by studying the memory capabilities of diurnal animals, particularly that of birds, which naturally rely on complex visuo-spatial cues in the wild for their survival.

There are three reasons why birds may prove to be particularly suitable animal models for determining the extent to which the rodent results can be extrapolated to humans and other diurnal animals. Like humans, birds are largely diurnal, with visual and auditory cues providing the dominant input to the creation of spatial maps. Second, they show remarkable memory capabilities which are known to be dependent upon the hippocampus (e.g. Sherry et al., 1992). Third, bird brains are capable of showing dramatic experience-dependent changes in association with learning. Although a few new nerve cells are continually being born in the mammalian hippocampus throughout life (e.g. Altman et al., 1973, Kaplan and Hinds, 1977, Bayer, 1982, Kempermann et al., 1997), the avian hippocampus is considerably more plastic. Experiences associated with the formation of new memories can trigger dramatic increases in the birth rate of new nerve cells that migrate to the avian hippocampus: the daily rate of neurogenesis in the ventricular zone (the germinal area of the adult avian brain) increases from 3.9% in control birds that were prevented from caching to 10% in experienced birds that had received three 20 min trials of caching and retrieval (Patel et al., 1997b). Thus, birds may be particularly good models for looking at mechanisms of brain plasticity, and how the hippocampus responds to memory-related experiences.

Learning and memory in songbirds has received attention from a diverse group of ethologists and neuroscientists. One paradigm involves the relationship between the volume of the avian hippocampus and memory in food-storing birds (e.g. Clayton and Krebs, 1995). While the details vary from species to species, an individual bird will store hundreds or even thousands of food items during the autumn and winter in numerous cache sites which are scattered throughout the home area; and successful cache retrieval depends at least in part on memory for individual cache sites, a memory which is formed during a single brief visit during which the item was hidden (e.g. Sherry et al., 1981, Shettleworth and Krebs, 1982Balda and Kamil 1989). Laboratory experiments demonstrate that food-storing birds show accurate retention of many different spatial locations of cache sites over long time periods, ranging from over 40 days in willow tits, Parus montanus, (Brodin and Eckman, 1994) to more than 270 days in Clark’s nutcrackers, Nucifraga columbiana, (Balda and Kamil, 1992). Lesion studies demonstrate that a region of the dorsomedial cortex known as the avian hippocampus plays a role in successful retrieval of stored food (Krushinskya, 1966, Sherry and Vaccarino, 1989). These two findings, namely that food-storing birds possess an accurate, long-lasting memory for spatial locations and which is dependent on an intact hippocampus, has led to the development of the food-storing system as a model for investigating fundamental questions about memory and the brain.

In terms of function, the avian and mammalian hippocampus share many similarities (Nadel, 1991), not least of which is the correlation between food-storing behavior and enlargement of the hippocampal formation discussed above. Lesion studies show that damage to the avian hippocampus impairs the learning of tasks which depend upon spatial cues, but has no effect on performance when non-spatial color cues are made available to the bird (Sherry and Vaccarino, 1989, Hampton and Shettleworth, 1996Patel et al. 1997aSanford et al., in press), namely the same types of learning shown to be dependent upon an intact hippocampus in rodents (Olton and Samuelson 1976O’Keefe and Nadel, 1978; but see Rawlins et al., 1993). A third similarity with mammalian studies of hippocampal function is that avian HF seems likely to be involved in memory acquisition and consolidation but is probably not the site of memory storage. In homing pigeons, lesions impair the acquisition of new information as opposed to the consolidation of established memories (reviewed by Bingman, 1993). Recent studies on the zebra finch hippocampus also indicate that inhibition of estrogen synthesis impairs learning, but not memory of a hippocampally-dependant task (Clayton et al., 1997a), and results in a decrease in hippocampal volume and dendritic arborization of Calbindin-positive neurons (Saldanha et al., 1997). Fourth, studies of hippocampal function in humans and primates have suggested that the hippocampus is important in various forms of long term memory (LTM) whereas short term memory (STM) does not depend upon an intact hippocampus (reviewed by Squire, 1992). To date, only one study has investigated the effects of lesions on LTM for cache sites in birds (Krushinskya, 1966): when long retention intervals separated the storage of seeds from the opportunity to retrieve them, Eurasian nutcrackers with lesions of the hyperstriatum (including HF) were significantly impaired in their attempts to retrieve. These results suggest that avian and mammalian hippocampus share striking functional similarities. Since the anatomical organization of HF is markedly different from that of the mammalian hippocampus, this raises the question of whether or not the two do a similar job but in different ways (Clayton and Krebs, 1995).

Section snippets

Food-storing birds have an anatomical specialization of the brain

Food-storing birds possess a neuroanatomical specialization: comparisons of diverse families of birds show that the avian hippocampus is larger, relative to overall brain and body size, and contains more neurons in species which store food than in those which do not (Krebs et al., 1989, Sherry et al., 1989). This relationship is also true in mammals, where scatter-hoarding kangaroo rats have larger relative hippocampal volumes than do closely related species which cache all their food in one

The question of homology

In order to justify drawing comparisons between the avian and the mammalian hippocampus it is important to address the issue of whether or not the two structures are homologous. Initially, there was considerable skepticism, largely because (a) little is known about the intracortical connections within the avian hippocampus, making comparisons of their connectivity nigh impossible; and (b) the avian hippocampus has a very different structural organization from that of the mammalian hippocampus.

Comparative cognition

Much of the recent work on memory and the hippocampus in food-caching birds has characterized which memory functions are enhanced when a brain region is enlarged. This ‘inverse neuropsychology’ approach (Shettleworth, 1995) uses the comparative method at two different levels: (a) between species, to test for species differences in memory associated with differences in the brain; and (b) within species, to determine the effects of experience on development of memory and the brain.

The remarkable

Food-storing birds remember more than just spatial location

Food-storing birds can also remember other information about the contents of the cache site in addition to its spatial location. Sherry (1984)demonstrated that black capped chickadees, P. atricapillus, cached dehusked sunflower seeds more readily than whole safflower seeds and recovered the preferred food-type caches first. Kamil and Balda, 1985, Kamil and Balda, 1990also showed that Clark’s nutcrackers retrieve preferred items first, and with a lower error rate than that for non-preferred

Experience-dependent changes in memory and the hippocampus

Recent work on the concomitant development of food-caching, memory and the hippocampus in juvenile food-storing parids suggests that there may be a direct relationship between hippocampal volume and memory (e.g. see reviews by Clayton and Krebs, 1995Clayton and Lee, in press). By giving hand-raised marsh tits the experience of storing and recovering food caches at different ages, and subsequently comparing the hippocampal volume of these birds with age-matched inexperienced birds, Clayton and

Neural mechanisms of learning and memory

What kinds of neuroanatomical changes account for the hippocampal volume increase? Hippocampal growth is correlated with an increase in the total numbers of neurons within the hippocampus, rather than with changes in cell size or density (Healy and Krebs, 1993Healy et al., 1994Clayton and Krebs, 1994c). Given the changes in neuron number, one critical question concerns the relative importance of cell birth and programmed cell death since the total number of hippocampal neurons is a function of

Does memory and the hippocampus change with age?

Given this plasticity in hippocampal morphology, an obvious question is whether the experience-dependent changes in the hippocampus are restricted to juveniles, or whether the adult hippocampus also grows and atrophies in response to food-caching experience (Clayton and Lee, in press). Barnea and Nottebohm (1994)have shown that there are seasonal peaks in neurogenesis in the autumn which coincide with a peak in food-caching intensity. However, it is not known if non-storing species also show

Acknowledgements

I thank Mike Caun, Emma Krebs, Georgina Krebs, Kirsten Sanford and Anthony Dickinson for help with the scrub jay experiments, and Jennifer Greig for her great bird care skills. I am indebited to Robert Gerlai, Richard Morris and two anonymous referees for thoughtful discussion and helpful comments on the manuscript. Financial support was provided by NIH, the Whitehall Foundation, University of California Alzheimer’s Disease Center, University of California Davis Faculty Research, and Bodega

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