Differential excitatory control of 2 parallel basket cell networks in amygdala microcircuits

摘要

Information processing in neural networks depends on the connectivity among excitatory and inhibitory neurons. The presence of parallel, distinctly controlled local circuits within a cortical network may ensure an effective and dynamic regulation of microcircuit function. By applying a combination of optogenetics, electrophysiological recordings, and high resolution microscopic techniques, we uncovered the organizing principles of synaptic communication between principal neurons and basket cells in the basal nucleus of the amygdala. In this cortical structure, known to be critical for emotional memory formation, we revealed the presence of 2 parallel basket cell networks expressing either parvalbumin or cholecystokinin. While the 2 basket cell types are mutually interconnected within their own category via synapses and gap junctions, they avoid innervating each other, but form synaptic contacts with axo-axonic cells. Importantly, both basket cell types have the similar potency to control principal neuron spiking, but they receive excitatory input from principal neurons with entirely diverse features. This distinct feedback synaptic excitation enables a markedly different recruitment of the 2 basket cell types upon the activation of local principal neurons. Our data suggest fundamentally different functions for the 2 parallel basket cell networks in circuit operations in the amygdala. Author summary The perisomatic region of neurons refers collectively to the membrane surface of the cell body or soma, proximal dendrites, and axon initial segment. This is a unique functional domain in which the activity of a neuron can be controlled in the most effective manner. In the cerebral cortex, the perisomatic region of excitatory principal cells is solely innervated by inhibitory interneurons, which can be divided into 3 functional groups: axo-axonic cells and 2 types of basket cells. The reason why 3 distinct types of inhibitory cells are specialized to control principal cell firing is still unknown. To reveal the possible differences in the role of the 3 interneuron types played in cortical operation, we have investigated the organizing principles of synaptic communication between principal cells and inhibitory cell types in the basal nucleus of the amygdala. In this cortical structure, known to be critical for affective behavior, we revealed that the 2 basket cell types avoid innervating each other but contact axo-axonic cells. Both basket cell types have a similar potency to control principal cell firing, but they receive excitatory input from principal cells with entirely distinct features. Our data suggest fundamentally different functions for the 2 parallel basket cell networks in amygdala operation.