A spatially structured network of inhibitory and excitatory connections directs impulse traffic within the lateral amygdala

Abstract

The lateral nucleus of the amygdala is the entry point of most sensory inputs into the amygdala. However, the way information is processed and distributed within the lateral nucleus still eludes us. To gain some insight into this issue, we have examined the spatial organization of excitatory and inhibitory connections in the lateral nucleus. To this end, we performed whole-cell recordings of principal lateral amygdala neurons and studied their responses to local pressure applications of glutamate in coronal and horizontal slices of the guinea-pig amygdala. In coronal sections, glutamate puffs performed at a distance from the recorded cells usually evoked inhibitory responses, except when the recorded neuron was adjacent to the external capsule, in which case excitatory responses could be evoked from ejection sites along the external capsule. In contrast, glutamate puffs evoked a mixture of excitatory and inhibitory responses in horizontal slices. Excitatory responses were generally evoked from stimulation sites located lateral to the recorded cell whereas inhibitory responses were commonly elicited from medial stimulation sites, irrespective of their rostrocaudal position. These findings confirm and extend previous tract-tracing studies where it was found that intrinsic connections within the lateral amygdala prevalently run in the dorsoventral and lateromedial directions. However, our results also reveal a hitherto unsuspected level of spatial heterogeneity in the intrinsic circuit of the lateral amygdala. The prevalence of excitatory responses in horizontal slices coupled to the ubiquity of inhibitory responses in coronal slices suggest that the lateral amygdala network is designed to allow associative interactions within the rostrocaudal plane while preventing runaway excitation locally.