Cortical-Like Functional Organization of the Pheromone-Processing Circuits in the Medial Amygdala

Abstract

The medial amygdala (MeA) is a critical center for processing pheromonal signals that regulate social and reproductive behaviors, but the fundamental cellular mechanisms underlying signal processing in the MeA have remained largely unknown. Some studies suggest that the MeA belongs to the striatum and provides inhibitory output to hypothalamic areas including the ventromedial hypothalamus (VMH). By combining tract tracing, genetic labeling of GABAergic neurons, and immunostaining against markers for glutamatergic synapses, we found that a majority of MeA neurons projecting to the VMH are glutamatergic. Whole cell patch-clamp recordings revealed that VMH-projecting neurons form a homogeneous population in terms of morphological and intrinsic properties. Nearly all cells possess I(h) and I(T) and in some cases they can give rise to postinhibitory rebound spikes. Morphological analysis of neurobiotin-filled cells revealed neurons with long dendritic arbors that extend to the MeA external layer and within the amygdala. Thus the VMH-projecting neurons in the MeA differ from the medium spiny neurons, the principal neurons of striatum, in terms of intrinsic physiological properties and morphology. In contrast, they resemble a subset of pyramidal cells in deep piriform cortex. Similar to pyramidal cells in piriform cortex, the VMH-projecting neurons in the MeA received direct excitatory input from their upstream sensory areas and inhibitory input from local GABAergic neurons. We conclude that pheromonal signals relayed to the VMH are processed by unique cortical, but not striatal, circuitry in the MeA.