Polarized synaptic interactions between intercalated neurons of the amygdala

The intercalated (ITC) cell masses are small GABAergic cell clusters interposed between the basolateral (BL) complex and central (CE) nucleus of the amygdala. ITC cells receive excitatory afferents from the BL complex and generate feed-forward inhibition in the CE nucleus. Recently it was shown that ITC cells could gate impulse traffic between the BL complex and CE nucleus in a spatiotemporally differentiated manner. In addition, it was hypothesized that lateromedial inhibitory interactions between different ITC cell clusters played a critical role in this respect. Given the potential importance of such conditional computations, the present study aimed to characterize the connectivity existing among ITC cells. To this end, whole cell recordings of ITC neurons were obtained under visual guidance in coronal slices of the guinea pig amygdala. Electrical stimuli applied in the BL complex primarily elicited excitatory responses when they were applied at the same lateromedial level or more medially than the recorded ITC cells. As the stimulation site was moved laterally, the character of the response shifted toward inhibition. Both bicuculline and non-N-methyl-D-aspartate receptor antagonists abolished this BL-evoked inhibition, suggesting that it was not mediated by BL inhibitory cells projecting to ITC neurons. In keeping with this, local glutamate injections in and around the ITC clusters revealed that the most effective site to inhibit ITC cells were ITC clusters located laterally with respect to the recorded one. The activation of more medial ITC clusters evoked much smaller responses. Thus, connections between ITC clusters tend to run in a lateromedial direction. To identify the source of these directionally polarized synaptic interactions, the morphological features of ITC cells were analyzed by intracellular injection of Neurobiotin. This analysis revealed that the dendritic tree and axonal arbor of ITC cells are asymmetric in the lateromedial plane. In particular, their laterally directed dendrites were longer than the medial ones, whereas their laterally directed axon collaterals were shorter than the medial ones. It is concluded that the morphological asymmetry of ITC cells accounts for the directional polarization of inter-ITC connections. The significance of these findings for the gating of information transfer from the BL complex to the CE nucleus is discussed.