David F. Sherry

The Evolution of Multiple Memory Systems

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. It allows them to take advantage of previous experience to help solve the multitude of problems with which their environment confronts them, such as how to recognize the familiar, predict events, return to particular places, and assess the consequences of behavior Recently the question has arisen as to whether the

The hippocampal complex of food-storing birds.

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.

Hippocampus and memory for food caches in black-capped chickadees.

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

Spatial memory and adaptive specialization of the hippocampus

The hippocampus plays an important role in spatial memory and spatial cognition in birds and mammals. Natural selection, sexual selection and artificial selection have resulted in an increase in the size of the hippocampus in a remarkably diverse group of animals that rely on spatial abilities to solve ecologically important problems. Food-storing birds remember the locations of large numbers of scattered caches. Polygynous male voles traverse large home ranges in search of mates. Kangaroo rats both cache food and exhibit a sex difference in home range size. In all of these species, an increase in the size of the hippocampus is associated with superior spatial ability. Artificial selection for homing ability has produced a comparable increase in the size of the hippocampus in homing pigeons, compared with other strains of domestic pigeon. Despite differences among these animals in their histories of selection and the genetic backgrounds on which selection has acted, there is a common relationship between relative hippocampal size and spatial ability.

Memory for the location of stored food in marsh tits

Abstract Marsh tits store several hundred food items per day, in separate locations within their territory, and recover most items within 24 h. Experiments in the laboratory determined that marsh tits return accurately to the sites of stored sunflower seeds 3 h and 24 h after storage. The proportion of returns exceeded chance encounter and initial preferences for those sites. The lack of interocular transfer in birds for some visual tasks provided a test for the hypothesis that memory is used to relocate stored food. After storing food with one eye covered, marsh tits did not return to storage sites when using only the ‘naive’ eye, but did so when using only the eye uncovered during storage. It seems likely that recovery of stored food by marsh tits and other birds occurs by memory of storage sites, not by chance encounter during foraging.

Food storing by marsh tits

Wild marsh tits (Parus palustris) were allowed to hoard radioactively labelled sunflower seeds, which were subsequently found using a portable scintillation counter. Seeds were stored singly, in various sites close to the ground. Different birds favoured different types of site, although this preference was changeable. Seed density decreased with increasing distance from the feeder, and there was a negative correlation between seed sequence number and the distance it was carried. Hoarded seeds disappeared more rapidly than control seeds in identical sites 100 cm away, suggesting that the birds remember their exact location. Seeds also tended to be stored and recovered in the same sequence. The adaptive significance of these results is discussed.

Food storage by black-capped chickadees: Memory for the location and contents of caches

Abstract Black-capped chickadees ( Parus atricapillus ) store food in a scattered distribution in their winter home range. Several hundred food items may be stored in a day, each in a separate cache site. Previous studies of marsh tits ( Parus palustris ) and nutcrackers ( Nucifraga spp.) have shown that spatial memory is used to relocate caches. Memory for storage sites, if used by black-capped chickadees, is predicted to have four properties. Birds should be able to: (1) accurately relocate cache sites, (2) recall which caches they have previously emptied, (3) recall which sites they have discovered empty (as a result of loss to other animals) and (4) recall what type of food is stored at a cache site. Laboratory experiments show that chickadees do incorporate these kinds of information in memory for cache sites.

Hippocampal volume and food-storing behavior are related in parids.

The size of the hippocampus has been previously shown to reflect species differences and sex differences in reliance on spatial memory to locate ecologically important resources, such as food and mates. Black-capped chickadees (Parus atricapillus) cached more food than did either Mexican chickadees (P. sclateri) or bridled titmice (P. wollweberi) in two tests of food storing, one conducted in an aviary and another in smaller home cages. Black-capped chickadees were also found to have a larger hippocampus, relative to the size of the telencephalon, than the other two species. Differences in the frequency of food storing behavior among the three species have probably produced differences in the use of hippocampus-dependent memory and spatial information processing to recover stored food, resulting in graded selection for size of the hippocampus.

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.

Evolution and the hormonal control of sexually-dimorphic spatial abilities in humans

A number of hypotheses have been proposed for the evolution of sex differences in spatial ability. Two of these hypotheses assume a sex-based division of labor in foraging during human evolutionary history, three propose sexual selection for spatial ability, and two suggest that human life history has imposed sex-specific selection on spatial abilities. We derive predictions from each of these models and test the predictions against recent data on the effects of hormones on spatial ability across the lifespan. Sexual selection for increased range size in males might be the evolutionary origin of the enhancing effects of testosterone on spatial ability, while the benefits of reduced mobility in women at different stages of reproduction could be the origin of the inhibitory effects of oestrogen on spatial ability.