In a study of 52 individuals belonging to 35 species or subspecies of passerine birds it was shown that the volume of the hippocampal complex relative to brain and body size is significantly larger in species that store food than in species that do not. Retrieval of stored food relies on an accurate and long-lasting spatial memory, and hippocampal damage disrupts memory for storage sites. The results suggest, therefore, that food-storing species of passerines have an enlarged hippocampal complex as a specialization associated with the use of a specialized memory capacity. Other lifehistory variables were examined and found not to be correlated with hippocampal volume.Some species of birds store large numbers offood items, each in a separate place, and use an accurate, long-lasting spatial memory to retrieve their stores (1-5). We show here that the hippocampal complex (dorsomedial forebrain) (6) of foodstoring passerines is larger relative to body and brain size than that of nonstorers. Thus, across a range of species, a relationship has been found between the structure of a specific brain area outside sensory and motor areas and a specific behavior. METHODSWe measured the volume of the hippocampal complex and striatum of52 individuals belonging to 35 species or subspecies distributed among 9 passerine families [taxonomy in this paper follows that of Sibley et al. (7) based on DNADNA hybridization]. We defined the hippocampal complex as including the closely interconnected hippocampal and parahippocampal areas (6). The evidence from both embryological and connectivity studies (8-10) suggests that these two structures as a whole are homologous to the mammalian hippocampal complex, although the homology ofthe different subdivisions is not known. The behavioral consequences of damage to the avian hippocampal complex show that it is broadly functionally equivalent to the mammalian hippocampus in playing an important role in certain memory tasks, including those involving spatial memory (11)(12)(13)(14)(15)(16)(17)(18). The avian hippocampal complex is a paired structure located adjacent to the midline of the dorsal telencephalon (19). It extends from the caudal limit of the striatum along approximately two-thirds of the caudal-rostral extent of the striatum. In coronal section it is bounded medially by the midline and ventrally by the lateral horns of the ventricle and by the septum (Fig. 1). The region defined as the hippocampus by Karten and Hodos (19) is a V-shaped structure of densely packed cells lying ventrally and medially (Fig. 1). In the parahippocampal area large and small neurons are sparsely and nonuniformly distributed. The lateral boundary of the parahippocampal area is characterized by a change in the size distribution of neurons. Medial to the boundary the distribution is bimodal with peaks at cell areas of about 20 pIm2 and 130-150 pum2, while lateral to the boundary the distribution is unimodal with a peak at about 20-30 ILm2 (Fig. 2): the boundary is often clearer in food-storers than i...
The existence of multiple memory systems has been proposed in a number of areas, including cognitive psychology, neuropsychology, and the study of animal learning and memory. We examine whether the existence of such multiple systems seems likely on evolutionary grounds. Multiple systems adapted to serve seemingly similar functions, which differ in important ways, are a common evolutionary outcome. The evolution of multiple memory systems requires memory systems to be specialized to such a degree that the functional problems each system handles cannot be handled by another system. We define this condition as functional incompatibility and show that it occurs for a number of the distinctions that have been proposed between memory systems. The distinction between memory for song and memory for spatial locations in birds, and between incremental habit formation and memory for unique episodes in humans and other primates provide examples. Not all memory systems are highly specialized in function, however, and the conditions under which memory systems could evolve to serve a wide range of functions are also discussed.Memory is a function that permits animals and people to acquire, retain, and retrieve many different kinds of information. We would like to thank Fergus Craik, Victoria Esses, Luc-Alain GiraIdeau, Robert Lockhart, David Olton, Paul Rozin, Sara Shettleworth, Larry Squire, Endel Tulving, and Derek Van der Kooy for their many helpful comments and Carol Macdonald for her help with preparation of this article.The order of authorship was determined by a coin toss at the Young Lok Restaurant, where most of the article evolved.Correspondence concerning this article should be addressed to David F. Sherry, Department of Psychology, University of Toronto, Toronto, Ontario, Canada M5S 1A1 or to Daniel L. Schacter, who is now at the Department of Psychology, University of Arizona, Tucson, Arizona 85721. 1978;Olton, Becker, & Handelmann, 1979;Rozin & Kalat, 1971;Schacter &Moscovitch, 1984;Shettleworth, 1972;Squire & Cohen, 1984;Tulving, 1983). Some researchers are not convinced of the need to postulate the existence of multiple memory systems, however, and maintain that the experimental evidence does not mandate rejecting the view of a unitary learning and memory system that is explainable by a single set of general principles or laws (Bitterman, 1975;Craik, 1983;Jacoby, 1983Jacoby, , 1984Kolers & Roediger, 1984;Logue, 1979;MacPhail, 1982;Revusky, 1977).The purposes of this article are to determine whether there are evolutionary grounds for favoring a unitary or a nonunitary view of memory and to bring together recent research on memory systems in humans and animals that bears on this problem. The principal question we address is whether the evolution of qualitatively distinct memory systems would be expected to occur or whether a single memory system that is characterized by increasing complexity and flexibility is the expected evolutionary outcome. We develop an argument that favors the former alternative and that...
Three families of North American passerines – chickadees, nuthatches and jays – store food. Previous research has shown that memory for the spatial locations of caches is the principal mechanism of cache recovery. It has also been previously shown that the hippocampal complex (hippocampus and area parahippocampalis) plays an important role in memory for cache sites. The present study determined the volume of the hippocampal complex and the telencephalon in 3 food-storing families and in 10 non-food-storing families and subfamilies of passerines. The hippocampal complex is larger in food-storing birds than in non-food-storing birds. This difference is greater than expected from allometric relations among the hippocampal complex, telencephalon and body weight. Food-storing families are not more closely related to each other than they are to non-food-storing families and subfamilies, and the greater size of the hippocampal complex in food-storing birds is therefore the result of evolutionary convergence. Natural selection has led to a larger hippocampal complex in birds that rely on memory to recover spatially dispersed food caches.
In a study of two congeneric rodent species, sex differences in hippocampal size were predicted by sexspecific patterns of spatial cognition. Hippocampal size is known to correlate positively with maze performance in laboratory mouse strains and with selective pressure for spatial memory among passerine bird species. In polygamous vole species (Rodentia: Microtus), males range more widely than females in the field and perform better on laboratory measures of spatial ability; both of these differences are absent in monogamous vole species. Ten females and males were taken from natural populations of two vole species, the polygamous meadow vole, M. pennsylvanicus, and the monogamous pine vole, M. pinetorum. Only in the polygamous species do males have larger hippocampi relative to the entire brain than do females. Two-way analysis of variance shows that the ratio of hippocampal volume to brain volume is differently related to sex in these two species. To our knowledge, no previous studies of hippocampal size have linked both evolutionary and psychometric data to hippocampal dimensions. Our controlled comparison suggests that evolution can produce adaptive sex differences in behavior and its neural substrate.The hippocampus, a large forebrain structure, plays an important role in spatial learning (1-3). Rodents given hippocampal lesions show impaired performance on spatial tasks (4-6), and spatial performance is positively correlated with certain hippocampal dimensions in inbred mouse strains (7-9). Hippocampal size also varies between males and females in laboratory rats (10) and across species (11,12). Recent evidence suggests that variation in hippocampal size among species may be adaptively related to interspecific differences in the intensity of selection for spatial processing: the hippocampus is relatively larger in birds that hoard food items in scattered locations than it is in avian species that do not use this spatially demanding foraging tactic (13-15). In general, ecological pressures are known to shape brain evolution (16)(17)(18). In this paper, we integrate field and laboratory data on spatial behavior with measures of hippocampal size to show that evolution may produce adaptive sex differences in particular brain structures.Likely candidates for neural sex differences are species known to exhibit adaptive sex differences in spatial ability. Spatial ability should evolve in proportion to the navigational demands that an individual faces in its natural environment. In most mammalian species, males and females exploit the same environment, but the patterns of competition for mates determine how the two sexes exploit this environment. In monogamous species, the sexes exhibit convergent reproductive strategies. They exploit the environment in similar ways and therefore are subject to similar selective pressures for spatial ability. Conversely, divergent reproductive strategies predominate in polygamous species. Here, range expansion is an important tactic used by polygamous males to maximize the...
Black-capped chickadees and other food-storing birds recover their scattered caches by remembering the spatial locations of cache sites. Bilateral hippocampal aspiration reduced the accuracy of cache recovery by chickadees to the chance rate, but it did not reduce the amount of caching or the number of attempts to recover caches. In a second experiment, hippocampal aspiration * dissociated performance of a task requiring memory for places from performance of a task requiring memory for cues associated with food, disrupting the former but not the latter. On both tasks, however, hippocmpal aspiration increased the frequency of revisiting errors to sites previously searched. These experiments show that the structure in the avian brain that is neuroanatomically and embryologically homologous to the mammalian hippocampus shares some functions with the mammalian hippocampus. The results indicate that memory for places and working memory are both disrupted by hippocampal damage in birds. Finally, it was possible to show that these memory capacities are essential for cache recovery by black-capped chickadees.Black-capped chickadees (Parus atricapillus) store food in concealed locations scattered throughout their home range. They store seeds and invertebrate prey, and they put each food item in a separate cache site. Hollow stems, crevices in bark, moss, leaf buds, dry leaves, and natural cavities are used as storage sites. Chickadees, and the congeneric marsh tit (Parus palustris), may store as many as several hundred food items per day and place neighboring caches at least several meters apart. They recover their stored food a few days after caching it, and in the wild they do not reuse cache sites Sherry, Avery, & Stevens, 1982;Stevens &Krebs, 1986). Stored food is recovered by remembering the spatial locations of caches (Cowie et al., 1981;Sherry, 1984a;Shettleworth & Krebs, 1982).The evidence that memory for spatial locations is the principal means of cache recovery comes from a number of experimental field and laboratory studies, reviewed by Sherry (1985). In the field, seeds are taken from cache sites at a higher rate than they are taken from identical control sites 10 cm away (Cowie et al., 1981). Although this is not unequivocal evidence of memory, it shows that cache recovery is spatially precise and is not based on exhaustive search of all sites resembling the cache site. An experiment in which This research was supported by the Natural Sciences and Engineering Research Council of Canada.We thank Alison Fleming, Michael Leon, Larry Squire, and Franco Vaccarino for their advice and encouragement, and Elisabeth Murray and Derek van der Kooy for their comments on an earlier draft of the manuscript. We are grateful to Karen Buckenham and Siegfried Schulte for their technical assistance and to Jim Hare for his help catching chickadees.
Neuroecology is the study of adaptive variation in cognition and the brain. The origin of neuroecology dates from the 1980s, when researchers in behavioral ecology began to apply the methods of comparative evolutionary biology to cognitive processes and the underlying neural mechanisms of cognition. The comparative approach, however, is much older. It was a mainstay of ethology, it has been part of the study of neuroanatomy since the seventeenth century, and it was used by Darwin to marshal evidence for the theory of natural selection. Neuroecology examines the relations between ecological selection pressures and species or sex differences in cognition and the brain. The goal of neuroecology is to understand how natural selection acts on cognition and its neural mechanisms. This chapter describes the general approach of neuroecology, phylogenetic comparative methods used in the field, and new findings on the cognitive mechanisms and brain structures involved in mating systems, social organization, communication, and foraging. The contribution of neuroecology to psychology and the neurosciences is the information it provides on the selective pressures that have influenced the evolution of cognition and brain structure.
Females of the brood-parasitic brown-headed cowbird (Molothrus ater) search for host nests in which to lay their eggs. Females normally return to lay a singe egg from one to several days after first locating a potential host nest and lay up to 40 eggs in a breeding season. Male brown-headed cowbirds do not assist females in locating nests. We predicted that the spatial abilities required to locate and return accurately to host nests may have produced a sex difference in the size of the hippocampal complex in cowbirds, in favor of females. The size of the hippocampal complex, relative to size of the telencephalon, was found to be greater in female than in male cowbirds. No sex difference was found in two closely related nonparasitic icterines, the red-winged blackbird (Agelaiusphoeniceus) and the common grackle (Quiscalusquiscula). Other differences among these species in parental care, migration, foraging, and diet are unlikely to have produced the sex difference attributed to search for host nests by female cowbirds. This is one of few indications, in any species, of greater speclalization for spatial ability in females and confirms that use of space, rather than sex, breeding system, or foraging behavior per se, can influence the relative size of the hippocampus.Brown-headed cowbirds (Molothrus ater) are brood parasites. During breeding, females lay a single egg early in the day and spend the remainder of the morning searching for host nests in which to lay eggs on subsequent days (1-3). Females feed in the afternoon, often leaving the breeding area to do so (1, 4). Females of the eastern subspecies that were the subjects of the present study, M. ater ater, lay at least 40 eggs over the course ofan 8-week breeding season (refs. 5 and 6; see also ref. 7). Male brown-headed cowbirds do not search for host nests or assist females in gaining access to host nests (7) but associate with females, both monogamously and polygamously, in breeding and feeding habitat. Field studies describe male association with females as consisting largely of following females during their daily activities (4).Female cowbirds have a variety of methods for locating host nests, including sitting silently and watching nestbuilding activity by potential hosts, walking on the forest floor while scanning the canopy, and flying into shrubs and low vegetation to flush hosts from their nests (8). Females do not lay in a host nest immediately upon locating it. Search for new host nests follows laying in the daily routine (9), and females are selective in their choice of host nest, preferring to lay in a completed nest containing at least one, but not more than two, host eggs (10, 11). Females must therefore return to the location of a previously discovered host nest in order to lay in it, one or more days after first locating the nest The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this f...
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