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Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning

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ABSTRACT

Sex differences in neurological disease exist in incidence, severity, progression, and symptoms and may ultimately influence treatment. Cognitive disturbances are frequent in neuropsychiatric disease with men showing greater cognitive impairment in schizophrenia, but women showing more severe dementia and cognitive decline with Alzheimer's disease. Although there are no overall differences in intelligence between the sexes, men, and women demonstrate slight but consistent differences in a number of cognitive domains. These include a male advantage, on average, in some types of spatial abilities and a female advantage on some measures of verbal fluency and memory. Sex differences in traits or behaviors generally indicate the involvement of sex hormones, such as androgens and estrogens. We review the literature on whether adult levels of testosterone and estradiol influence spatial ability in both males and females from rodent models to humans. We also include information on estrogens and their ability to modulate verbal memory in men and women. Estrone and progestins are common components of hormone therapies, and we also review the existing literature concerning their effects on cognition. We also review the sex differences in the hippocampus and prefrontal cortex as they relate to cognitive performance in both rodents and humans. There has been greater recognition in the scientific literature that it is important to study both sexes and also to analyze study findings with sex as a variable. Only by examining these sex differences can we progress to finding treatments that will improve the cognitive health of both men and women. © 2016 American Physiological Society. Compr Physiol 6:1295‐1337, 2016.

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Figure 1. Figure 1. Tasks favoring women or men. On average women show superior performance in tasks requiring perceptual speed, verbal fluency, visual memory, and fine motor skills compared to men. However, men tend to do better than women on spatial tasks such as the mental rotations test, the paper‐folding test, embedded figures, and have better target accuracy even when accounting for sports history. Figure adapted from Figures and with permission from Kimura 1992 ().
Figure 2. Figure 2. Morris water maze task. Theoretical data arising from male and female rodents in the Morris water maze task. The Morris water maze task is a hippocampus dependent task that is widely used to study spatial learning and memory. Typically in the reference memory version of the task, animals learn the location of a hidden platform located just beneath the surface of the water, over successive trial days, in the context of extra maze cues located around the room. Before the location of the platform is learned, animals take longer and swim a greater distance to find the platform, but once the location is encoded to memory, animals typically swim directly to the platform when placed in the maze. Males typically outperform females on the reference version of this task in a variety of rodents (). Intriguingly performance is disrupted in females when landmarks (extra maze cues) are disorganized whereas male performance is disputed when changing the geometric properties of the room compared to the maze [i.e., circular versus square ‐ curtains around the maze versus no curtains—see ()].
Figure 3. Figure 3. Hippocampal anatomy. A drawing illustrating the local circuitry in the hippocampus, which is referred to as the trisynaptic circuit. Cells in layer two of the entorhinal cortex send projections, via the perforant pathway, to granule neurons in the granule cell layer of the dentate gyrus (DG). Granule neurons project to pyramidal neurons in the CA3 cell layer via the mossy fiber pathway. CA3 pyramidal neurons send projections to CA1 pyramidal neurons via the Shaffer Collaterals. CA1 pyramidal neurons then project back to layer 5 of the entorhinal cortex (EC). Each neuronal population uses an excitatory synaptic connection to stimulate postsynaptic neurons in the circuit. Thus, the flow of information arising from the EC is sent to the DG, then the CA3, which sends it to CA1 neurons and then back to the EC.
Figure 4. Figure 4. Androgen and estrogen receptor (ER) distribution in the hippocampus. Both ERα and ERβ are found in CA1, CA3, and the DG of the adult male and female rodent hippocampus. The androgen (AR) is expressed in CA1 and CA3, but not in the DG of adult male and female rodents, with an exception in Wistar rats.
Figure 5. Figure 5. Estrogen receptor (ER) signaling. Estradiol can bind to the membrane receptor GPER or can crosses into the cell and binds with cytoplasmic or nuclear ERs of which there are two isoforms (ER α or β). Once bound, ERα or β undergoes a conformational change and dimerizes with another bound ER (forming hetero‐ or homodimers). The complex is transported into the nucleus and binds with estrogen response elements (EREs) in the DNA to initiate transcription of estrogen responsive genes or directly interacts with a transcription factor (TF) such as AP‐1 to initiate transcription of estrogen responsive genes. Once the mRNA is produced, the message is exported back to the soma and the protein is assembled. Adding to the complexity of signaling, coregulators, either coactivators or corepressors, interact with the bound ER to alter gene expression. Bound G‐protein‐coupled estrogen receptor (GPER) activates a second messenger cascade and increases the activity of several kinases, which in turn activate transcription factors to initiate transcription.
Figure 6. Figure 6. Classic genomic response of the androgen receptor (AR). Testosterone crosses into the soma of the cell and binds with and AR. Once bound, the AR undergoes a conformational change and dimerizes with another bound AR. The complex is transported into the nucleus and binds with and ARE to initiate transcription of androgen responsive genes. Once the mRNA is produced, the message is exported back to the soma and the protein is assembled.


Figure 1. Tasks favoring women or men. On average women show superior performance in tasks requiring perceptual speed, verbal fluency, visual memory, and fine motor skills compared to men. However, men tend to do better than women on spatial tasks such as the mental rotations test, the paper‐folding test, embedded figures, and have better target accuracy even when accounting for sports history. Figure adapted from Figures and with permission from Kimura 1992 ().


Figure 2. Morris water maze task. Theoretical data arising from male and female rodents in the Morris water maze task. The Morris water maze task is a hippocampus dependent task that is widely used to study spatial learning and memory. Typically in the reference memory version of the task, animals learn the location of a hidden platform located just beneath the surface of the water, over successive trial days, in the context of extra maze cues located around the room. Before the location of the platform is learned, animals take longer and swim a greater distance to find the platform, but once the location is encoded to memory, animals typically swim directly to the platform when placed in the maze. Males typically outperform females on the reference version of this task in a variety of rodents (). Intriguingly performance is disrupted in females when landmarks (extra maze cues) are disorganized whereas male performance is disputed when changing the geometric properties of the room compared to the maze [i.e., circular versus square ‐ curtains around the maze versus no curtains—see ()].


Figure 3. Hippocampal anatomy. A drawing illustrating the local circuitry in the hippocampus, which is referred to as the trisynaptic circuit. Cells in layer two of the entorhinal cortex send projections, via the perforant pathway, to granule neurons in the granule cell layer of the dentate gyrus (DG). Granule neurons project to pyramidal neurons in the CA3 cell layer via the mossy fiber pathway. CA3 pyramidal neurons send projections to CA1 pyramidal neurons via the Shaffer Collaterals. CA1 pyramidal neurons then project back to layer 5 of the entorhinal cortex (EC). Each neuronal population uses an excitatory synaptic connection to stimulate postsynaptic neurons in the circuit. Thus, the flow of information arising from the EC is sent to the DG, then the CA3, which sends it to CA1 neurons and then back to the EC.


Figure 4. Androgen and estrogen receptor (ER) distribution in the hippocampus. Both ERα and ERβ are found in CA1, CA3, and the DG of the adult male and female rodent hippocampus. The androgen (AR) is expressed in CA1 and CA3, but not in the DG of adult male and female rodents, with an exception in Wistar rats.


Figure 5. Estrogen receptor (ER) signaling. Estradiol can bind to the membrane receptor GPER or can crosses into the cell and binds with cytoplasmic or nuclear ERs of which there are two isoforms (ER α or β). Once bound, ERα or β undergoes a conformational change and dimerizes with another bound ER (forming hetero‐ or homodimers). The complex is transported into the nucleus and binds with estrogen response elements (EREs) in the DNA to initiate transcription of estrogen responsive genes or directly interacts with a transcription factor (TF) such as AP‐1 to initiate transcription of estrogen responsive genes. Once the mRNA is produced, the message is exported back to the soma and the protein is assembled. Adding to the complexity of signaling, coregulators, either coactivators or corepressors, interact with the bound ER to alter gene expression. Bound G‐protein‐coupled estrogen receptor (GPER) activates a second messenger cascade and increases the activity of several kinases, which in turn activate transcription factors to initiate transcription.


Figure 6. Classic genomic response of the androgen receptor (AR). Testosterone crosses into the soma of the cell and binds with and AR. Once bound, the AR undergoes a conformational change and dimerizes with another bound AR. The complex is transported into the nucleus and binds with and ARE to initiate transcription of androgen responsive genes. Once the mRNA is produced, the message is exported back to the soma and the protein is assembled.
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Dwayne K. Hamson, Meighen M. Roes, Liisa A. M. Galea. Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning. Compr Physiol 2016, 6: 1295-1337. doi: 10.1002/cphy.c150031