Estrogen control of central neurotransmission: Effect on mood, mental state, and memory

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Abstract

1. Estrogen exerts profound effects on mood, mental state and memory by acting on both "classical" monoamine and neuropeptide transmitter mechanisms in brain. Here we review an example of each type of action. 2. With respect to the effect of estrogen on central monoamine neurotransmission, low levels of estrogen in women are associated with the premenstrual syndrome, postnatal depression and post-menopausal depression. Sex differences in schizophrenia have also been attributed to estrogen. Previous studies have shown that estrogen stimulates a significant increase in dopamine2 (D2) receptors in the striatum. Here we show for the first time that estrogen also stimulates a significant increase in the density of 5-hydroxytryptamine2A (5-HT2A) binding sites in anterior frontal, cingulate and primary olfactory cortex and in the nucleus accumbens, areas of the brain concerned with the control of mood, mental state, cognition, emotion and behavior. These findings explain, for example, the efficacy of estrogen therapy or 5-HT uptake blockers such as fluoxetine in treating the depressive symptoms of the premenstrual syndrome. and suggest that the sex differences in schizophrenia may also be due to an action of estrogen mediated by way of 5-HT2A receptors. 3. With respect to the effect of estrogen on central neuropeptide transmission, estrogen stimulates the expression of the arginine vasopressin (AVP) gene in the bed nucleus of the stria terminalis (BNST) in rodents. This results in a 100-fold increase in AVP mRNA in the BNST and a massive increase in AVP peptide in the BNST and its projections to the lateral septum and lateral habenula. The BNST-AVP system enhances and/or maintains "social" or "olfactory" memory, and thus provides a powerful model for correlating transcriptional control of neuropeptide gene expression with behavior. Whether similar mechanisms operate in the human remain to be determined. 4. These two examples of the action of estrogen on central neurotransmission are discussed in terms of their immediate clinical importance for the treatment of depressive symptoms, their use as powerful models for investigations on the steroid control of central neurotransmitter mechanisms, and the role of estrogen as "Nature's" psychoprotectant.

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Most cited references 60

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Although many workers have appreciated the striking cytologic and neurochemical similarities of neostriatum, accumbens and olfactory tubercle, a compelling case for regarding these areas as territories in a striatal complex awaited the arguments made by Heimer and his colleagues based on their investigations of connections. A number of recent papers support this viewpoint and extend it with the characterization of three accumbal subterritories: core, shell and rostral pole. The case for separate classifications of systems traversing the accumbens has become more compelling with each study that demonstrates connectional, cytoarchitectural and neurochemical specificity conforming to the boundaries separating the core and its downstream targets from the shell and its projection fields. Furthermore, its apparent composite of core-like and shell-like characteristics distinguishes the rostral pole as yet another unique subterritory. Differences in compartmental organization distinguish the accumbens and neostriatum. The available data are consistent with the periventricular and rostrolateral enkephalin-rich zones being ventralmost parts of the neostriatal patch and matrix compartments, respectively. The accumbal cell cluster compartment, on the other hand, appears to be a separate entity, with connectional and neurochemical features that are dissimilar to both patch and matrix of neostriatum. Boundaries between the accumbens and caudate-putamen remain elusive, and the point of view that such boundaries do not exist but, rather, are represented by "transition zones" must to a large degree reflect the reality. Likewise, it is important to acknowledge that the boundaries between accumbal subterritories are not necessarily distinct or observed faithfully by all of the afferent systems. "Transition zones" appear to be particularly significant organizational features in rostral and lateral parts of the accumbens. Interestingly, histochemically distinct cell clusters tend to be numerous in boundary regions between adjacent territories and subterritories. The predominant organizational pattern appears to be one in which the core, shell and rostral pole engage different forebrain systems that possibly subserve entirely different functions mediated by distantly related mechanisms. In this regard, it is of paramount interest that the processing of information conveyed to the accumbens by diverse cortical and subcortical inputs occurs within distinct and perhaps very different dopaminergic environments in the core, shell and rostral pole (e.g., see Refs 24, 34, 90, 110).

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The distribution of serotonin-2 (5-HT2) receptors in the rat brain was studied by light microscopic quantitative autoradiography. Receptors were labeled with four ligands: [3H]ketanserin, [3H]mesulergine, [3H]LSD and [3H]spiperone, which are reported to show high affinity for 5-HT2 receptors. Co-incubation with increasing concentrations of several well-known 5-HT2-selective drugs, such as pirenperone, cinanserin and ketanserin, resulted in an inhibition of the binding of the four 3H-labeled ligands to the same areas. However, all of them recognized, in addition to 5-HT2 sites, other populations of binding sites. Receptor densities were quantified by microdensitometry with the aid of a computer-assisted image-analysis system. Our results reveal a heterogeneous distribution of 5-HT2 receptor densities in the rat brain. Very high concentrations were localized in the claustrum, olfactory tubercle and layer IV of the neocortex. The anterior olfactory nucleus, piriform cortex and layer I of neocortex were also rich in 5-HT2 receptors. Intermediate concentrations of receptors were found in caudate putamen, nucleus accumbens, layer V of neocortex, ventral dentate gyrus and mammillary bodies. Areas containing only low concentrations of receptors included the thalamus, hippocampus, brainstem, medulla, cerebellum and spinal cord. The specificity of the different ligands used is discussed in terms of the other populations of sites recognized by them. The distribution of 5-HT2 receptors here reported is discussed in correlation with (a) the known distribution of serotoninergic terminals, (b) the specific anatomical systems and (c) the central effects reported to be mediated by 5-HT2-selective drugs.

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Affective and psychotic symptoms associated with anabolic steroid use.

H Pope, D L Katz (1988)

To assess the frequency of affective and psychotic symptoms in athletes taking anabolic steroids, the authors performed structured interviews of 41 body-builders and football players who had used steroids. According to DSM-III-R, nine subjects (22%) displayed a full affective syndrome, and five (12%) displayed psychotic symptoms in association with steroid use. These findings suggest that major psychiatric symptoms may be a common adverse effect of these drugs.