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

• Published in: Journal of comparative neurology (1911) Vol. 522; no. 9; pp. 2075 - 2088
• Main Authors: Brusco, Janaina, Merlo, Suélen, Ikeda, Érika T., Petralia, Ronald S., Kachar, Bechara, Rasia-Filho, Alberto A., Moreira, Jorge E.
• Format: Journal Article
• Language: English
• Published: United States Blackwell Publishing Ltd 15.06.2014; Wiley Subscription Services, Inc
• Subjects: 3D reconstruction; Amygdala - physiology; Amygdala - ultrastructure; Animals; Axons - physiology; Axons - ultrastructure; Dendrites - physiology; Dendrites - ultrastructure; Dendritic Spines - physiology; Dendritic Spines - ultrastructure; electron microscopy; Estrous Cycle - physiology; extended amygdala; Female; Functional Laterality - physiology; gamma-Aminobutyric Acid - metabolism; Gap Junctions - physiology; Gap Junctions - ultrastructure; Imaging, Three-Dimensional; inhibitory dendritic spines; laterality; Male; Microscopy, Electron, Transmission; multisynaptic dendritic spines; Neural Inhibition - physiology; Neurons - physiology; Neurons - ultrastructure; Presynaptic Terminals - physiology; Presynaptic Terminals - ultrastructure; Rats, Wistar; Sex Characteristics; Synapses - physiology; Synapses - ultrastructure; Synaptic Vesicles - physiology; Synaptic Vesicles - ultrastructure; electron microscopy; extended amygdala; 3D reconstruction; inhibitory dendritic spines; laterality; multisynaptic dendritic spines
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23518

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 3D 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 nonsynaptic filopodia occur in the MePD. On average, 8.6% of dendritic spines received inputs from symmetric gamma‐aminobutyric acid (GABA)‐immunoreactive terminals, whereas 3.6% received two synaptic contacts on the spine head, neck, or base. Presynaptic terminals in female 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 estrous cycle phase in mature MePD neurons. Most likely, sexual hormone 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. J. Comp. Neurol. 522:2075–2088, 2014. © 2013 Wiley Periodicals, Inc. Combining serial‐section and immunocytochemical techniques for transmission electron‐microscopy, this work demonstrates spines with inhibitory and multiple synapses in the posterodorsal medial amygdala. The right hemisphere of females exhibits higher synaptic activity than the left hemisphere, while males show no laterality and less docked synaptic vesicles than the left hemisphere of females.