Microglia and neurons in the hippocampus of migratory sandpipers.

The semipalmated sandpiper Calidris pusilla and the spotted sandpiper Actitis macularia are long- and short-distance migrants, respectively. C. pusilla breeds in the sub-arctic and mid-arctic tundra of Canada and Alaska and winters on the north and east coasts of South America. A. macularia breeds in a broad distribution across most of North America from the treeline to the southern United States. It winters in the southern United States, and Central and South America. The autumn migration route of C. pusilla includes a non-stop flight over the Atlantic Ocean, whereas autumn route of A. macularia is largely over land. Because of this difference in their migratory paths and the visuo-spatial recognition tasks involved, we hypothesized that hippocampal volume and neuronal and glial numbers would differ between these two species. A. macularia did not differ from C. pusilla in the total number of hippocampal neurons, but the species had a larger hippocampal formation and more hippocampal microglia. It remains to be investigated whether these differences indicate interspecies differences or neural specializations associated with different strategies of orientation and navigation.

Microglia and neurons in the hippocampus of migratory sandpipers

The semipalmated sandpiper Calidris pusilla and the spotted sandpiper Actitis macularia are long- and short-distance migrants, respectively. C. pusilla breeds in the sub-arctic and mid-arctic tundra of Canada and Alaska and winters on the north and east coasts of South America. A. macularia breeds in a broad distribution across most of North America from the treeline to the southern United States. It winters in the southern United States, and Central and South America. The autumn migration route of C. pusilla includes a non-stop flight over the Atlantic Ocean, whereas autumn route of A. macularia is largely over land. Because of this difference in their migratory paths and the visuo-spatial recognition tasks involved, we hypothesized that hippocampal volume and neuronal and glial numbers would differ between these two species. A. macularia did not differ from C. pusilla in the total number of hippocampal neurons, but the species had a larger hippocampal formation and more hippocampal microglia. It remains to be investigated whether these differences indicate interspecies differences or neural specializations associated with different strategies of orientation and navigation.

A system for the automated recording of feeding behavior and body weight.

A method that uses passive integrated transponder (PIT) tags for the continuous recording of feeding behavior and body weight from multiple individual animals is described. We have used this method in the field and in semi-natural captive conditions with black-capped chickadees (Poecile atricapillus) to determine daily and seasonal patterns in body weight and to estimate the proportions of food cached and consumed.

Cross-species comparisons.

Cognitive and neural adaptations in animals have been analysed using the comparative method. Comparisons between closely related species that differ in a cognitive or neural character, and comparison between distantly related species that share a cognitive or neural character, can be used to identify adaptations. Recent research has identified adaptive modifications of memory and the hippocampus that have evolved convergently in two clades of food-storing birds, the chickadees and tits (Paridae), and the jays and nutcrackers (Corvidae). Similar modifications of the hippocampus occur in other groups of animals, such as the cowbird brood parasites, in which there has been selection for spatial memory. Three general patterns that emerge from the comparative study of animal cognition provide a framework for research on human psychological adaptations: the existence of both specialized and general cognitive capacities; a clear relation between specialized capacities and specific selective pressures; and evolutionary change in the relative size of brain areas with cognitive functions.

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.

Sex and intrauterine position influence the size of the gerbil hippocampus.

Sex differences in home range size and spatial ability are predictive of sex differences in the relative size of the hippocampus in rodents. Such differences in behavior and hippocampal volume are presumed to be, in part, the result of differences in perinatal exposure to hormones. We predicted from differences in the size of home ranges of male and female Mongolian gerbils (Meriones unguiculatus) in the wild that the hippocampus of male gerbils would be relatively larger than that of females. We examined the effect of prenatal hormonal influences on hippocampal size by comparing hippocampal volume of males and females from 2F and 2M intrauterine positions to that of randomly selected males and females. We found that, as predicted, randomly selected males had a significantly larger hippocampus, relative to telencephalon, than did randomly selected females. However, males and females from 2F and 2M intrauterine positions did not differ in relative hippocampal size. Possible explanations for the absence of a sex difference in hippocampal size in male and female gerbils from 2F and 2M intrauterine positions are discussed.

No sex difference occurs in hippocampus, food-storing, or memory for food caches in black-capped chickadees.

A number of recent studies have described sex differences in the relative size of the hippocampus that are associated with sex differences in the use of space. Voles, kangaroo rats, and cowbirds all exhibit a sex difference in relative size of the hippocampal formation that is correlated with a sex difference in spatial behaviour. We wished to determine whether sex differences in the size of the hippocampus occur in the absence of a difference in the use of space, and whether the previously described correlations could be adventitious. Relative hippocampal size was determined in wild-caught black-capped chickadees (Parus atricapillus) following behavioural observations of food caching and spatial memory for cache sites. There was no indication of a sex difference in either relative size of the hippocampus or in food-caching behaviour and memory for cache sites. These results show that sex differences in relative size of the hippocampus do not occur as a matter of course, and are consistent with the hypothesis that sex differences in spatial behaviour and spatial ability are predictive of sex differences in the relative size of the hippocampus.

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.

Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird.

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 single 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 (Agelaius phoeniceus) and the common grackle (Quiscalus quiscula). 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 specialization 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.

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.

Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.

In a study of two congeneric rodent species, sex differences in hippocampal size were predicted by sex-specific 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.

Hippocampal specialization of food-storing birds.

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 life-history variables were examined and found not to be correlated with hippocampal volume.

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.

Animal anorexias.

Eating very little in the presence of food or failure to serach for food has been documented in various species during the hibernation season, incubation, molting, and defense of the territory or harem. At these times feeding competes with other, more important activities. One way to avoid conflicts between feeding and these other activities to lower the programmed weight or set-point for body fat. Experiments on mammalian hibernators and incubating birds provide evidence that set-points are indeed lowered. Failure to eat in these two examples depends on anorexia, loss of appetite. A review of other examples suggests that conceptualization in terms of lowered set-points provides a unified and testable way of understanding many naturally occurring instances of fasting in the animal kingdom. Finally, spontaneous animal anorexias are contrasted with attempts by people to lose weight.