Inhibitory and multisynaptic spines, and hemispherical synaptic specialization in the posterodorsal medial amygdala of male and female rats

Abstract

The density of dendritic spines is sexually dimorphic and variable throughout the female estrous cycle in the rat posterodorsal medial amygdala (MePD), a relevant area for the modulation of reproductive behavior in rats. The local synaptic activity differs between hemispheres in prepubertal animals. Here, we used serial section transmission electron microscopy to produce three-dimensional reconstructions of dendritic shafts and spines to characterize synaptic contacts on MePD neurons of both hemispheres in adult males and in females along the estrous cycle. Pleomorphic spines and non-synaptic filopodia occur in the MePD. On average, 8.6% of dendritic spines received inputs from symmetric GABA-immunoreactive terminals, whereas 3.6% received two synaptic contacts on the spine head, neck or base. Presynaptic terminals in females right MePD had a higher density of synaptic vesicles and docked vesicles than the left MePD, suggesting a higher rate of synaptic vesicle release in the right MePD of female rats. In contrast, males did not show laterality in any of those parameters. The proportion of putative inhibitory synapses on dendritic shafts in the right MePD of females in proestrus was higher than in the left MePD, and higher than in the right MePD in males, or in females in diestrus or estrus. This work shows synaptic laterality depending on sex and the estrous cycle phases in mature MePD neurons. Most likely, sexual hormones effects are lateralized in this brain region, leading to higher synaptic activity in the right than in the left hemisphere of females, mediating timely neuroendocrine and social/reproductive behavior.

Remodeling of the number and structure of dendritic spines in the medial amygdala: From prepubertal sexual dimorphism to puberty and effect of sexual experience in male rats

“…Then, from the 3D reconstructed images, spines were classified and counted according to morphological criteria based on spine length (SL), neck length (NL), neck diameter (ND), head diameter (HD) and the number of protrusions from a single stalk (Dall'Oglio, Dutra, Moreira, & Rasia‐Filho, ; Zancan et al., and references therein). Based on their shapes, spines were classified into the following: (a) thin (when SL > HD and HD > ND), (b) mushroom‐like (HD ≫ ND), (c) stubby/wide (HD > SL), (d) ramified (with a single stalk that branches in two heads) or (e) atypical (when showing a transitional aspect between classes or an unusual shape not classified in the other classes (based on Arellano, Benavides‐Piccione, DeFelipe, & Yuste, ; Brusco et al., , ; Dall'Oglio et al., ; Harris et al., ; Stewart, Popov, Kraev, Medvedev, & Davies, ; Zancan et al., and references therein). Representative examples are shown in Figures and .…”

The human medial amygdala: structure, diversity, and complexity of dendritic spines

“…We also looked for the presence and shape of spinules (smaller protrusions usually extending from the head of a spine; Brusco et al. ; Stewart et al. ) and filopodium (a thin and elongated protrusion with no apparent head; García‐López et al.…”

“…It was not possible to obtain 150–300 ultra‐thin serial sections to perform 3D reconstructions of TEM images from our samples as obtained for rats or mice (see Fiala & Harris, ; Brusco et al. ; Stewart et al. ).…”

“…; Brusco et al. ). Spines have varied shapes, sizes, and functions (Holtmaat & Svoboda, ; García‐López et al.…”

Hypothesis: CeM–RVLM circuits may be implicated in sudden unexpected death in epilepsy by melanocortinergic–sympathetic signaling

“…Liu et al used immunolabeling against glial fibrillary acidic protein (GFAP) and green fluorescent protein for fluorescence immunohistochemical detection and assayed GFAPimmunoreactivity (GFAP-ir) in adult male MC4R-GFP transgenic mice [9]. They reported that GFAP-ir cells were mainly labeled in the medial subdivision of the central amygdala (CeM) and sparsely distributed in the lateral subdivision of the central amygdala (CeL) and basolateral amygdala (BLA) [9], suggesting that the CeM is a major subdivision in the amygdala which participates in the regulation of astrocytic activity [11][12][13]. This observation was in line with previous evidence indicating a possible local restructuring of astrocytic cytoskeleton in the medial amygdala after myocardial infarction/heart failure in rats [14].…”