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The lateral (LA) and basolateral (BL) nuclei of the amygdala regulate emotional behaviors. Despite their dissimilar extrinsic connectivity, they are often combined, perhaps because their cellular composition is similar to that of the cerebral cortex, including excitatory principal cells reciprocally connected with fast-spiking interneurons (FSIs). In the cortex, this microcircuitry produces gamma oscillations that support information processing and behavior. We tested whether this was similarly the case in the rat (males) LA and BL using extracellular recordings, biophysical modeling, and behavioral conditioning. During periods of environmental assessment, both nuclei exhibited gamma oscillations that stopped upon initiation of active behaviors. Yet, BL exhibited more robust spontaneous gamma oscillations than LA. The greater propensity of BL to generate gamma resulted from several microcircuit differences, especially the proportion of FSIs and their interconnections with principal cells. Furthermore, gamma in BL but not LA regulated the efficacy of excitatory synaptic transmission between connected neurons. Together, these results suggest fundamental differences in how LA and BL operate. Most likely, gamma in LA is externally driven whereas in BL, it can also arise spontaneously to support ruminative processing and the evaluation of complex situations. SIGNIFICANCE STATEMENT: The basolateral amygdala (BLA) participates in the production and regulation of emotional behaviors. It is thought to perform this using feedforward circuits that enhance stimuli that gain emotional significance and directs them to valence-appropriate downstream effectors. This perspective overlooks the fact that its microcircuitry is recurrent and potentially capable of generating oscillations in the gamma band (50-80 Hz), which synchronize spiking activity and modulate communication between neurons. This study found that BLA gamma supports both these processes, is associated with periods of action selection and environmental assessment irrespective of valence, and differs between BLA subnuclei in a manner consistent with their heretofore unknown microcircuit differences. Thus, it provides new mechanisms for BLA to support emotional behaviors.

Gamma oscillations in the basolateral amygdala: localization, microcircuitry, and behavioral correlates