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...

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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...