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

Abstract

The posterodorsal medial amygdala (MePD) is a sexually dimorphic area and plays a central role in the social behavior network of rats. Dendritic spines modulate synaptic processing and plasticity. Here, we compared the number and structure of dendritic spines in the MePD of prepubertal males and females and postpubertal males with and without sexual experience. Spines were classified and measured after three-dimensional image reconstruction using DiI fluorescent labeling and confocal microscopy. Significantly differences are as follows: (a) Prepubertal males have more proximal spines, stubby/wide spines with long length and large head diameter and thin and mushroom spines with wide neck and head diameters than prepubertal females, whereas (b) prepubertal females have more mushroom spines with long neck length than age-matched males. (c) In males, the number of thin spines reduces after puberty and, compared to sexually experienced counterparts, (d) naive males have short stubby/wide spines as well as mushroom spines with reduced neck diameter. In addition, (e) sexually experienced males have an increase in the number of mushroom spines, the length of stubby/wide spines, the head diameter of thin and stubby/wide spines and the neck diameter of thin and mushroom spines. These data indicate that a sexual dimorphism in the MePD dendritic spines is evident before adulthood and a spine-specific remodeling of number and shape can be brought about by both puberty and sexual experience. These fine-tuned ontogenetic, hormonally and experience-dependent changes in the MePD are relevant for plastic synaptic processing and the reproductive behavior of adult rats.

Sexual dimorphism, estrous cycle and laterality determine the intrinsic and synaptic properties of medial amygdala neurons in rat

“…Here, we recorded cells from the MePD, avoiding the ultimate borders of this subnucleus (de Olmos et al, 2004;Nishizuka and Arai, 1983a,b). Third, the two subpopulations of adult rat MePD neurons were multipolar spiny cells, confirming previous morphological data (Cooke et al, 2007;Dall'Oglio et al, 2008;Rasia-Filho et al, 2004;Zancan et al, 2018). Different from the MeA of mice, we have not observed pyramidal (Niimi et al, 2012) or pyramidal-like (Bian, 2013) neurons in the MePD of rats (Marcuzzo et al, 2007).…”

“…MePD. These data reinforce the plastic changes in dendritic spines and synaptic processes in the MePD after puberty in rats (Cooke and Woolley, 2009;Zancan et al, 2018). On the other hand, the mEPSCs in MePD neurons of prepubertal rats have a higher frequency on the left, but not the right, hemisphere in males compared to females (Cooke and Woolley, 2005).…”

“…The posterodorsal subdivision of the medial nucleus of the amygdala (MePD) expresses high levels of androgen, progesterone, and both estrogen αand β-receptors (Gréco et al, 1998;de Vries and Simerly, 2002;Frankiensztajn et al, 2018). This relates to the occurrence of a local sexual dimorphism and the effects of sex steroids, evidenced by structural and functional differences in prepubertal and adult male and female rats (Cooke and Woolley, 2005;Morris et al, 2008;Rasia-Filho et al, 2004;Zancan et al, 2018). The MePD modulates the display of reproductive behavior in both sexes (Adekunbi et al, 2018), mainly intromission and ejaculation in males (Coolen and Wood, 1999;Coolen et al, 1997;Rasia-Filho et al, 2012a), or the timely secretion of gonadotrophin-releasing hormone for ovulation (Polston et al, 2001;Simerly, 2004) and display of sexual behavior in females (Pfaus and Heeb, 1997;Polston et al, 2001).…”

“…They were classified as bitufted or stellate cells, with two or more than two primary dendrites emerging from an ovoid to round cell body, respectively (Dall'Oglio et al, 2008;Rasia-Filho et al, 2004). This cellular homogeneity might explain the low variability of data obtained for the quantification of soma size, soma volume and dendritic spine density of Golgi-impregnated neurons from the MePD of male rats (Rasia-Filho et al, 2012a;Zancan et al, 2017Zancan et al, , 2018.…”

Role of the posterodorsal medial amygdala in predator odour stress‐induced puberty delay in female rats

“…The MeA, particularly its posterodorsal subnucleus (MePD) receives olfactory information from environmental and sexual cues, which are relayed to the medial preoptic area (mPOA) where the gonadotrophin‐releasing hormone (GnRH) neurones are located to bring about the appropriate reproductive response. The MePD also undergoes dramatic anatomical changes during puberty and exerts a regulatory role on puberty timing, as indicated by studies in rats showing that MePD lesions caused puberty advancement, whereas its electrical stimulation delayed puberty onset . In addition, the MePD has been implicated in ovulation and oestrous cyclicity, as well as gonadotrophic hormone secretion …”