Lucia F. Jacobs

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.

The Evolution of Self-Control

Significance Although scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problem-solving tasks measuring self-control and evaluated the leading hypotheses regarding how and why cognition evolves. Across species, differences in absolute (not relative) brain volume best predicted performance on these tasks. Within primates, dietary breadth also predicted cognitive performance, whereas social group size did not. These results suggest that increases in absolute brain size provided the biological foundation for evolutionary increases in self-control, and implicate species differences in feeding ecology as a potential selective pressure favoring these skills. Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Unpacking the cognitive map: The parallel map theory of hippocampal function

In the parallel map theory, the hippocampus encodes space with 2 mapping systems. The bearing map is constructed primarily in the dentate gyrus from directional cues such as stimulus gradients. The sketch map is constructed within the hippocampus proper from positional cues. The integrated map emerges when data from the bearing and sketch maps are combined. Because the component maps work in parallel, the impairment of one can reveal residual learning by the other. Such parallel function may explain paradoxes of spatial learning, such as learning after partial hippocampal lesions, taxonomic and sex differences in spatial learning, and the function of hippocampal neurogenesis. By integrating evidence from physiology to phylogeny, the parallel map theory offers a unified explanation for hippocampal function.

How does cognition evolve? Phylogenetic comparative psychology

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Grey squirrels remember the locations of buried nuts

Abstract It has previously been assumed that grey squirrels, Sciurus carolinensis , cannot remember the locations of nuts they have buried, and hence must relocate nuts by their odour. This assumption was tested by measuring the accuracy of cache retrieval of captive squirrels. Each squirrel was released alone into an outdoor arena, where it cached 10 hazelnuts. After a delay of 2,4 or 12 days, each squirrel was returned to the arena and tested for its ability to retreve nuts from its own cache sites and from 10 cache sites used by other squirrels. Although each squirrels own caches were close to the caches of other squirrels, the squirrels retrieved significantly more nuts from their own sites than from sites used by other squirrels, after all delays. The retrieval accuracy of the squirrels under these conditions indicates that while grey squirrels can locate buried nuts by their odour, they can also remember the individual locations of nuts they have buried.

Natural Space-Use Patterns and Hippocampal Size in Kangaroo Rats

The size of the hippocampus, a forebrain structure that processes spatial information, correlates with the need to relocate food caches by passerine birds and with sex-specific patterns of space use in microtine rodents. The influences on hippocampal anatomy of sexual selection within species, and natural selection between species, have not yet been studied in concert, however. Here we report that natural space-use patterns predict hippocampal size within and between two species of kangaroo rats (Dipodomys). Differences in foraging behavior suggest that Merriams kangaroo rats (D. merriami) require better spatial abilities than bannertail kangaroo rats (D. spectabilis). Sex-specific differences in mating strategy suggest that males of both species require more spatial ability than females. As predicted, hippocampal size (relative to brain size) is larger in Merriams than in bannertail kangaroo rats, and males have larger hippocampi than females in both species. Males of a third species (D. ordii) also have smaller hippocampi than Merriams kangaroo rat males, despite being similar to Merriams in brain and body size. These results suggest that both natural and sexual selection affect the relative size and perhaps function of mammalian hippocampi. They also reassert that measures of functional subunits of the brain reveal more about brain evolution than measures of total brain size.

The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels

The dentate gyrus is one of two areas in the mammalian brain that produces neurons in adulthood. Neurogenesis (proliferation, survival, and differentiation of new neurons) is regulated by experience, and increased neurogenesis appears to be correlated with improved spatial learning in mammals and birds. We tested the hypothesis that in long‐lived mammals that scatter‐hoard food, seasonal variations in spatial memory processing (i.e. increased processing during caching season in the autumn) might correlate with changes in neurogenesis and neuron number in the granule cell layer of the dentate gyrus (gcl DG). We investigated the rate of cell proliferation and the total number of neurons in the granule cell layer of wild adult eastern grey squirrels (Sciurus carolinensis) at three different times of the year (October, January and June). We found no seasonal differences in cell proliferation rate or in total neuron number in the granule cell layer. Our findings are in agreement with those of previous studies in laboratory mice and rats, and in free‐ranging, food‐caching, black‐capped chickadees, as well as with current hypotheses regarding the relationship between neurogenesis and learning. Our results, however, are also in agreement with the hypothesis that neurogenesis in the dentate gyrus represents a maintenance system that may be regulated by environmental factors, and that changes in total neuron number previously reported in rodents represent developmental changes rather than adult plasticity. The patterns observed in mature wild rodents, such as free‐ranging squirrels, may represent more accurately the extent of hippocampal plasticity in adult mammals.

Sexual selection and the brain

Sex differences are intrinsically interesting, particularly in the brain. When sexually dimorphic structures mediate learning, and when such learning ability is necessary to compete for mates, then such differences are best understood within the framework of sexual selection. By categorizing recent studies of sex differences in the brain by their role in mate competition, theories of sexual selection can be used to predict and characterize the occurrence of dimorphisms among species with different mating systems.

From chemotaxis to the cognitive map: The function of olfaction

A paradox of vertebrate brain evolution is the unexplained variability in the size of the olfactory bulb (OB), in contrast to other brain regions, which scale predictably with brain size. Such variability appears to be the result of selection for olfactory function, yet there is no obvious concordance that would predict the causal relationship between OB size and behavior. This discordance may derive from assuming the primary function of olfaction is odorant discrimination and acuity. If instead the primary function of olfaction is navigation, i.e., predicting odorant distributions in time and space, variability in absolute OB size could be ascribed and explained by variability in navigational demand. This olfactory spatial hypothesis offers a single functional explanation to account for patterns of olfactory system scaling in vertebrates, the primacy of olfaction in spatial navigation, even in visual specialists, and proposes an evolutionary scenario to account for the convergence in olfactory structure and function across protostomes and deuterostomes. In addition, the unique percepts of olfaction may organize odorant information in a parallel map structure. This could have served as a scaffold for the evolution of the parallel map structure of the mammalian hippocampus, and possibly the arthropod mushroom body, and offers an explanation for similar flexible spatial navigation strategies in arthropods and vertebrates.

Memory for cache locations in Merriam's kangaroo rats

Abstract The ability of Merriams kangaroo rats, Dipodomys merriami , to remember the location of food caches and to relocate caches in the absence of the odour of buried seeds was examined. Eight wild-caught kangaroo rats cached seeds in an experimental arena, and retrieved them 24 h, later. Before retrieval, all odours associated with the cache sites were removed and seeds were replaced in only half of the cache sites. During retrieval, kangaroo rats were significantly more likely to search cache sites, with or without seeds, than non-cache sites. Non-cache sites were primarily investigated after all cache sites had been searched, indicating that search of non-cache sites did not denote an error in cache retrieval. These results suggest that kangaroo rats can remember the locations of food caches, and can relocate cache sites even when there is no odour of buried seeds. To estimate the advantage enjoyed by the forager with greater information, a second experiment compared an owners success in retrieving its caches with the success of naive kangaroo rats searching for these same caches. Nine wild-caught kangaroo rats were allowed to search for caches that were distributed in the same spatial pattern as that created by one kangaroo rat from the first experiment. The naive subjects found significantly fewer caches than had the cache owner in the same length of time. This suggests that the use of spatial memory by a Merriams kangaroo rat to relocate its food caches gives it a competitive advantage over other kangaroo rats that may be searching for its caches.