Abstract
The generation of emotional responses by the amygdala is determined largely by the balance of excitatory and inhibitory inputs to its principal neurons. These responses are often sex-specific, and any imbalance in excitatory and/or inhibitory tones leads to serious psychiatric disorders which occur with different rates in men versus women. To investigate the neural basis of sex-specific processing in the amygdala, relationships between the neurons expressing calbindin (CB), parvalbumin (PV) and calretinin (CR), which form in the amygdala main subsets of γ-aminobutyric acid (GABA)-ergic inhibitory system, and neurons endowed with oestrogen alpha (ERα), oestrogen beta (ERβ) or androgen (AR) receptors were analysed using double immunohistochemistry in male and female guinea pig subjects. The results show that in various nuclei of the amygdala in both sexes small subsets of CB neurons and substantial proportions of PV neurons co-express ERβ, while many of the CR neurons co-express ERα. Both these oestrogen-sensitive populations are strictly separated as CB and PV neurons almost never co-express ERα, while CR cells are usually devoid of ERβ. In addition, in the medial nucleus and some other neighbouring regions, there are non-overlapping subpopulations of CB and CR neurons which co-express AR. In conclusion, the localization of ERα, ERβ or AR within subsets of GABAergic interneurons across diverse amygdaloid regions suggests that steroid hormones may exert a significant influence over local neuronal activity by directly modulating inhibitory tone. The control of inhibitory tone may be one of the mechanisms whereby oestrogen and androgen could modulate amygdala processing in a sex-specific manner. Another mechanism may be thorough steroid-sensitive projection neurons, which are most probably located in the medial and central nuclei.
Highlights
Populations of endowed with oestrogen alpha (ERa)?, ERb? and AR? neurons had slightly different patterns of distribution in the amygdala, these three patterns had many common features (Figs. 1, 2). In both sexes, the ERa?, ERb? and AR? cells were the most numerous and the most densely packed in the medial nucleus (Figs. 1, 2)
To the best of our knowledge, the present study describes for the first time a systematic analysis of relationships between populations of CB?, PV? and CR? neurons, which form in the amygdala main subsets of GABA? system and neurons bearing steroid receptors such as ERa or ERb or AR
The localization of ERa, ERb or AR within subsets of GABAergic interneurons across diverse amygdaloid regions suggests that steroid hormones may exert a significant influence over local neuronal activity by directly modulating inhibitory tone
Summary
The amygdala is composed of a set of nuclei and cortical regions within the temporal lobe which are thought to be critically important for emotional behaviour and emotional learning (LeDoux 2003; Sah et al 2003; Pape and Pare 2010), mediation of pheromonal and reproductive functions (Baum 2009; Kevetter and Winans 1981; Martel and Baum 2009; Morris et al 2008; Segovia et al 2006), drug addiction mechanisms (Buffalari and See 2010) and stress response (LeDoux 1994). Women on average retain stronger and more vivid memories of emotional events than men (Seidlitz and Diener 1998; Canli et al 2002). The fact that emotional memories tend to be stronger in women may be linked to the greater prevalence of depression and some types of anxiety disorders in women (Bekker and van Mens-Verhulst 2007; Davidson et al 2002). There are many other psychological disorders involving emotional function which occur with substantially different rates in men versus. Anorexia is another disorder associated with amygdala dysfunction, which is observed more often in women than in men (Swaab et al 2003). Schizophrenia, autism and drug addiction, associated with abnormalities in the functioning of the amygdala, are quoted more frequently in men than in women (Swaab et al 2003). It is worth mentioning that various aspects of amygdala anatomy are sexually dimorphic (Morris et al 2008; Rowniak 2013; Rowniak et al 2015; Segovia et al 2006)
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