The neurons expressing calcium-binding proteins in the amygdala of the guinea pig: precisely designed interface for sex hormones

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.

Evidence of altered depression and dementia‐related proteins in the brains of young rats after ovariectomy

“…A recent study in the AMY of the guinea pig reported that in various nuclei of the AMY, small subsets of CB neurons and substantial proportions of PV neurons co‐express ERβ, whereas many of the CR neurons co‐express ERα. Both of these estrogen‐sensitive populations are strictly separated, as CB and PV neurons almost never co‐express ERα, whereas CR cells are usually devoid of ERβ (Równiak ). By western blotting, we observed that ERα and ERβ both were decreased in the AMY of the OVX rats.…”

Regional chemoarchitecture of the brain of lungfishes based on calbindin D‐28K and calretinin immunohistochemistry

“…The distinct distribution of CB and CR in the amygdaloid complex has been analyzed in diverse vertebrates and, specially in mammals, has served to subdivide these structures (Sorvari, Soininen, & Pitkanen, ,b; Kemppainen & Pitkanen, ; Ashwell, Hardman, & Paxinos, ; Legaz et al, ; Równiak, ). Nevertheless, there is a great variability in the specific content of CB and CR in each amygdaloid nucleus among species, which makes difficult the use of the distribution of calcium binding proteins as a criterion for comparison.…”

Ontogeny of Neurons Containing Calcium‐Binding Proteins in the Preoptic Area of the Guinea Pig: Sexually Dimorphic Development of Calbindin

“…Even though the exact physiological function of CB, CR, and PV is still not completely understood, they have been demonstrated to be important markers of separate neuronal populations in the adult brain (Arai et al ., ; Baimbridge et al ., ; Andressen et al ., ; Najdzion et al ., ; Równiak et al ., ; Wasilewska et al ., ; Hermanowicz‐Sobieraj et al ., ) and during brain ontogeny (Solbach and Celio, ; Zakowski and Robak, 2013; Hermanowicz‐Sobieraj and Robak, ). In the guinea pig, these proteins mark the vast majority of GABAergic neurons in amygdala, septum, and subicular complex (Równiak et al ., ; Wasilewska et al ., ; Hermanowicz‐Sobieraj and Robak, ; Równiak, ). In the amygdala neurons expressing CB and/or PV are sexually dimorphic and PV+ and CB+ neurons co‐express estrogen receptors beta (ERβ), while CR+ neurons co‐express estrogen receptors alpha (ERα) (Równiak et al ., ; Równiak, ).…”

“…In the guinea pig, these proteins mark the vast majority of GABAergic neurons in amygdala, septum, and subicular complex (Równiak et al ., ; Wasilewska et al ., ; Hermanowicz‐Sobieraj and Robak, ; Równiak, ). In the amygdala neurons expressing CB and/or PV are sexually dimorphic and PV+ and CB+ neurons co‐express estrogen receptors beta (ERβ), while CR+ neurons co‐express estrogen receptors alpha (ERα) (Równiak et al ., ; Równiak, ). Both these estrogen‐sensitive populations are strictly separated as PV+ and CB+ neurons almost never co‐express ERα while CR+ cells are devoid of ERβ (Równiak, ).…”

“…In the amygdala neurons expressing CB and/or PV are sexually dimorphic and PV+ and CB+ neurons co‐express estrogen receptors beta (ERβ), while CR+ neurons co‐express estrogen receptors alpha (ERα) (Równiak et al ., ; Równiak, ). Both these estrogen‐sensitive populations are strictly separated as PV+ and CB+ neurons almost never co‐express ERα while CR+ cells are devoid of ERβ (Równiak, ). Moreover, CR functions as a marker for immature neurons during the guinea pig brain development and it may be used for defining fetal stages in the septum and anterior thalamic nuclei (Zakowski and Robak, ; Hermanowicz‐Sobieraj and Robak, ).…”