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In essentially every domain of neuroscience, the generally implicit assumption that few, if any, meaningful differences exist between male and female brain function is being challenged. Here we address how this development is influencing studies of the neurobiology of learning and memory. While it has been commonly held that males show an advantage on spatial tasks, and females on verbal tasks, there is increasing evidence that sex differences are more widespread than ly supposed. Differing performance between the sexes have been observed on a of common learning tasks in both the human and animal literature, many neither purely spatial nor verbal.

We Innis LA sex dating sex differences reported in various areas to date, while attempting to identify common features of sexually dimorphic tasks, and to place these differences in a neurobiological context. This discussion focuses on studies of four classes of memory tasks for which sex differences have been frequently reported: spatial, verbal, autobiographical, and emotional memory.

We conclude that the female verbal advantage extends into numerous tasks, including tests of spatial and autobiographical abilities, but that a small but ificant advantage may exist for general episodic memory. We further suggest that for some tasks, stress evokes sex differences, which are not normally observed, and that these differences are mediated largely by interactions between stress and sex hormones.

Sex influences on brain function are ubiquitous.

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Differences between the sexes have been documented at every level of neuroscience, from single neurons in cell culture to systems level processes as measured by neuroimaging. In some cases, consideration of sex may ificantly alter, even reverse, conclusions about brain function drawn from the study of one sex alone Cahill In some fields, such as the study of drug addiction, the evidence for sex differences is so strong that consideration of sex as a factor is becoming the norm, rather than the exception Wetherington The claim that these neurobiological sex differences extend to the behavioral level has typically been more controversial.

Still, given how broadly sex differences are distributed on the neural level, it seems unlikely that their behavioral effects would be restricted solely to these domains. One area of behavior not considered in Hyde's review is the influence of sex on learning and memory. It is becoming increasingly clear, however, that an understanding of the neurobiological and cognitive consequences of sex is relevant across this field. In the review that follows, behavioral evidence indicating differences between men and women from numerous memory tasks will be considered.

We will argue that the effects of sex on memory depend critically on the kinds of memory being studied, with some tasks favoring males, while others favor females. We will further argue that the traditionally accepted view that males show an advantage in spatial processing while females excel at verbal tasks presents an incomplete picture Maccoby and Jacklin In particular, evidence will be presented that the male spatial advantage does not apply to some spatial tasks, and that the female advantage in verbal processing extends into many memory tasks which are not explicitly verbal.

Furthermore, evidence will be presented for ificant sex differences in the way that stress and arousal modulate memory formation. As many studies of the neurobiology of memory have yielded differing, even opposing, effects between the sexes, experimental des that do not consider potential sex differences risk producing incomplete, or incorrect, conclusions.

Sex can even be an important factor in situations for which no behavioral sex difference is evident. As will be discussed, substantial evidence suggests that for some tasks males and females may use differing neural paths to reach the same behavioral end point. Although reports of sex differences in learning and memory are not a new phenomenon, with some evidence dating to the beginnings of experimental psychology, recent neurobiological findings have renewed interest in the issue.

This fact, combined with increasing sophistication in examining sex influences on the psychological level, means the field is now much better positioned to move from simply documenting observed sex differences in learning and memory, to understanding the ways in which psychological level differences arise from their neural underpinnings. In discussing behavioral sex differences, we include effect sizes wherever the published studies provided enough information to compute them. We do so for two reasons. First, effect sizes may be useful in identifying commonalities across sex differences: Sex effects of similar size found across varying studies might suggest that a common, sexually dimorphic cognitive faculty is at work.

Second, there remains a widespread misconception in neuroscience that sex differences are uniformly small Cahill As we will show, sex effects range from the trivial to the very large, depending on the specific task being tested, as in the case for most domains of neuroscience. Hence, our goal will be to address the most prominent sex differences in multiple forms of learning and memory, highlighting the differences in the way sex affects different aspects of memory-related cognition, and attempting to place these in a neurobiological context.

Although we will focus primarily on human studies, in large part because much of this discussion will involve verbal and episodic memory, we also discuss evidence from animal work, and note where commonalities across species are observed. It will be rightly observed that the classifications of types of memory used in this review in several cases overlap, and that some may draw upon abilities not generally thought of as mnemonic. Spatial rotation, for example, is considered by many to be a working memory task Zimmer in that it requires the representation of a figure viewed from multiple angles to be held in memory and manipulated, and employs many of the same brain regions involved in prototypical Innis LA sex dating memory tasks Schendan and Stern However, some would argue that such spatial ability draws on specific neural systems devoted only to spatial processing, distinct from those employed in working memory tasks Logie Innis LA sex dating Thus, while rotation does seem to engage working memory, it also seems to require processes distinct to visual imagery, and determining the relative contributions of these forms of processing to the task is difficult.

Similarly, although autobiographical memory, as measured by long-term retrospective recollection of one's life, is presented separately in this review, autobiographical tasks certainly draw on episodic memory, along with semantic information. Likewise, both autobiographical memory and episodic memory, measured in the Innis LA sex dating term, likely involve substantial verbalization. Many of the tasks classified as verbal memory in this review, particularly word list recall, can also be understood as episodic, as these abilities are likely tightly intertwined.

The organization of this work, therefore, is not intended as taxonomy of memory processes. Indeed, no complete taxonomy of this sort is agreed upon in the field. Rather than organizing the sections of this paper by theoretical memorywe have divided it by specific memory tasks, in the hope that this will facilitate ease of reference.

Each of the sections of this review represents a distinct literature, with characteristic methods and tasks used to measure performance. It is hoped that this approach will allow researchers in each of these fields to easily find what is known about sex differences for the particular measures of memory that they study. We will attempt to some degree to separate the contributions of different of memory to different tasks, and to establish which tasks draw on common or distinct faculties. However, when we argue that two sex differences are distinct, we intend only to imply that these memory tasks should be treated as separate insofar as they are influenced by sex.

For example, given consistent evidence of female advantages on verbal tasks, we suggest that a common sex difference contributes to sex differences in performance on verbal recall tasks, episodic, and object memory tasks. We remain agnostic, however, as to what extent the processing underlying these tasks may be neurally or functionally separated. In most of the studies to be described, the researchers did not have access to information on gender, but instead assumed that this variable matched the more observable data that they did have, regarding biological sex.

However, biological sex and gender are not always aligned. Thus, we restrict our discussion to the observable variable, and make no assumptions regarding gender. Our discussion begins with a brief historical perspective, followed by a review of some relevant neurobiological sex differences in brain regions and processes known to be involved in learning and memory.

We next consider sex differences in two domains in which they have been most commonly observed—spatial and verbal memory—with particular attention to recent experiments showing telling exceptions to the commonly accepted pattern seen in studies on this topic.

Next, we will review the evidence for sex differences in autobiographical memory, with a particular interest in the notion that these differences represent a more general sex difference in episodic memory. Next, we will consider the influence of sex on the modulation of memory by emotional arousal and stress. We will argue that sex differences may be particularly evident in the study of emotional memory, in part because of newly discovered interactions between stress and sex hormones in memory.

Finally, we will briefly address some intriguing new directions that the field of sex differences is taking, driven by new methodologies. The publication in of Hermann Ebbinghaus' famous investigation of his own memory is generally taken as the start of modern memory investigations. Recognition of sex differences in memory followed shortly thereafter, when the British psychologist Havelock Ellis published what is considered the first large-scale study of biological and psychological sex differences. Many investigations followed.

And as might be expected from the study of any two presumably overlapping yet offset populations in which many variables, known and unknown, will influence experimental findings, the literature often appeared confusing, with some studies reporting sex differences in a particular condition, others reporting none. By the time of Maccoby and Jacklin's landmark summary of sex differences on the psychological level, interest in the topic appears to have been waning, in part because sex differences in brain and behavior were considered anathema by the political zeitgeist of the time Eagly et al.

Despite this largely negative conclusion, and despite the political zeitgeist, reports of sex differences in various aspects of memory, or in cognitive processes dependent upon memory, persisted. Renewed interest today in the issue of sex influences in memory appears driven heavily by neurobiological investigations, which have identified numerous sex differences in brain related to memory. In particular, neuroimaging has revealed Innis LA sex dating neural networks underlying task performance between the sexes, both for tasks where performance differs and where performance is equivalent Grabowski et al.

Interestingly, one can find sex effects in some early studies of the neurobiology of memory, although these seem by and large to have been forgotten.

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For example, McGaugh and Thomson investigated the effects of a stimulant strychnine on foot shock-motivated maze learning in male and female rats. Indeed, it is only much more recently that studies of memory in both male and female animals appear to be gradually returning. Neurobiological sex differences in brain regions implicated in learning and memory exist at multiple levels of analysis, from gross neuroanatomy to circuit properties to the molecular mechanisms underlying them. Before focusing on sex differences explicitly tied to memory, we will first briefly describe some of these neurobiological sex differences through which these differences could potentially be mediated.

Multiple studies report larger whole brain volumes in men than women Peters ; Allen et al. The volume of numerous brain structures, including many well known to be involved in learning Innis LA sex dating memory have also been found to differ ificantly between the sexes. Both post-mortem and imaging studies have found that relative to brain size, women have larger volumes in the hippocampus Filipek et al. In contrast, the relative volumes of the amygdala Giedd et al.

Interestingly, an analysis of numerous brain structures showing sexual dimorphism indicates that the magnitude of sex differences in the size of human brain structures correlates with the degree to which the regions express sex steroid receptors during development, as inferred from animal studies Goldstein et al.

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In addition to morphological differences, ificant sex differences exist in the metabolism of multiple neurotransmitters known to play an important role in cognition. Several studies show that the availability of dopamine transporters, which regulate synaptic dopamine levels, is ificantly greater in women than in men Lavalaye et al. Similarly, in the striatum, a structure well known to be involved in habit learning, female presynaptic dopamine levels exceed those of age-matched males Laakso et al.

Amphetamine-induced release of dopamine in the globus pallidus is also larger in women Riccardi et al. Plasma serotonin levels are also higher in women than in men Ortiz et al. These global differences reflect the aggregate effect of numerous local neurochemical sex differences. The male advantage in 5-HT2 receptors seems to derive particularly from frontal and cingulate cortices Biver et al. Microdialysis in rodents indicates that extracellular levels of both serotonin and dopamine in the amygdala are elevated in males relative to females, although females show a ificantly Innis LA sex dating serotonin response to stress Mitsushima et al.

While sex differences in dopamine seem to be insensitive to menstrual position, serotonergic sex differences do seem to be influenced by ovarian hormones. Exogenous sex hormone replacement ificantly enhances 5-HT2a binding throughout the cortex Moses et al.

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