Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus).

Gaulin, Steven J. C.; FitzGerald, Randall W.; Wartell, Matt S.

doi:10.1037/0735-7036.104.1.88

Cited by 88 publications

(55 citation statements)

References 31 publications

(49 reference statements)

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“…Researchers have also argued that there is an inverse relationship between spatial ability and exploratory/ambulatory behavior (e.g., Beatty, 1979). Although several studies have reported that female rats that make more errors on maze tasks also display higher locomotor behavior in a novel environment than do male animals (e.g., Stewart, Skvarenina, & Pottier, 1975), others have obtained no such relationship (Gaulin, FitzGerald, & Wartell, 1990;Seymour et al, 1996). Our data do address this issue.…”

Section: Discussionmentioning

confidence: 95%

The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats

Tees

1999

Dev. Psychobiol.

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Section: Discussionmentioning

confidence: 95%

The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats

Tees

1999

Dev. Psychobiol.

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“…No direct test of this hypothesis exists for rats, but it can be rejected for voles, where the more error-prone sex is less, not more, active during maze testing (42). Thus, the available data on rats and voles suggest that particular mating systems foster sexually dimorphic ranging patterns, whereas other mating systems foster monomorphism in both naturalistic behavior and psychometric performance.…”

Section: Introductionmentioning

confidence: 97%

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

Jacobs

Gaulin

Sherry

et al. 1990

Proc. Natl. Acad. Sci. U.S.A.

334

212

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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...

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“…For example, in comparison with monogamous voles, promiscuous voles develop more rapidly in their overall brain growth (Gutierrez et al, 1989) and in the development of specific central systems, such as brain-derived neurotrophic factor (Liu et al, 2001b). Female meadow voles are induced to undergo behavioral estrus more rapidly after exposure to a conspecific male (Taylor et al, 1992) and appear to perform better in navigational mazes (Gaulin et al, 1990) compared with female prairie voles. Monogamous and promiscuous voles also differ in their neuropeptide systems, such as vasopressin and oxytocin (Insel and Shapiro, 1992;Wang et al, 1997b), and such differences appear to underlie their ability to form and express pair bonding behavior (Insel and Hulihan, 1995;Liu et al, 2001a).…”

mentioning

confidence: 97%

Estrogen regulation of cell proliferation and distribution of estrogen receptor‐α in the brains of adult female prairie and meadow voles

Fowler

Johnson

Wang

2005

J of Comparative Neurology

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Adult female prairie (Microtus ochrogaster) and meadow (M. pennsylvanicus) voles were compared to examine neural cell proliferation and the effects of estrogen manipulation on cell proliferation in the amygdala, ventromedial hypothalamus (VMH), and dentate gyrus of the hippocampus (DG). Unlike prior studies, our study focused on the amygdala and VMH, because they are involved in social behaviors and may underlie behavioral differences between the species. Meadow voles had a higher density of cells labeled with the cell proliferation marker 5-bromo-2'-deoxyuridine (BrdU) in the amygdala and DG than did prairie voles. Treatment with estradiol benzoate (EB) for 3 days increased the density of BrdU-labeled cells in the amygdala, particularly in the posterior cortical (pCorA) and medial (pMeA) nuclei, in meadow, but not prairie, voles. Furthermore, the majority of the BrdU-labeled cells in the pCorA and pMeA displayed either a neuronal or a glial progenitor phenotype, but no species or treatment differences were found in the percentage of neuronal or glial progenitor cells. To understand better estrogen's effects on adult neurogenesis, we also examined estrogen receptor-alpha (ERalpha) distribution. Meadow voles had more ERalpha-labeled cells in the pCorA and VMH, but not in the pMeA or DG, than did prairie voles. In addition, more than one-half of the BrdU-labeled cells in the amygdala of both species coexpressed ERalpha labeling. Together, these data indicate that estrogen alters cell proliferation in a species- and region-specific manner, and some of these effects may lie in the specific localization of estrogen receptors in the adult vole brain.

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Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus).

Cited by 88 publications

References 31 publications

The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats

The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats

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

Estrogen regulation of cell proliferation and distribution of estrogen receptor‐α in the brains of adult female prairie and meadow voles

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