Abstract
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.
Highlights
Gamma-aminobutyric acid (GABA)ergic basket and axo-axonic cells (AACs) targeting the perisomatic region of cortical principal neurons (PNs) are in a key position to effectively control the firing of their postsynaptic partners [1, 2]
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
In the basal amygdala (BA), cholecystokininexpressing basket cells (CCKBCs) and parvalbumincontaining basket cells (PVBC) innervate their own kind as in other cortical regions [20,21,22,23,24], we performed paired whole-cell recordings from 2 interneurons in slices prepared from mice expressing red fluorescent protein under the control of the Cck promoter (CCK-DsRed) and from mice which expressed enhanced green fluorescent protein under the control of the Pvalb promoter (PV-eGFP), respectively [37]
Summary
Gamma-aminobutyric acid (GABA)ergic basket and axo-axonic cells (AACs) targeting the perisomatic region of cortical principal neurons (PNs) are in a key position to effectively control the firing of their postsynaptic partners [1, 2]. While previous work uncovered that cholecystokininexpressing basket cells (CCKBCs) and parvalbumin-containing basket cells (PVBCs) innervate their own kind [20,21,22,23,24], it is still unclear whether the 2 BC types target each other, giving rise to a “super-network” of BCs that could very efficiently regulate spiking of their target neurons, primarily supervising the local circuit operation They may form 2 parallel GABAergic networks without any synaptic cross-talk, a circuit organization that could substantially increase the adjustability and computational power in cortical networks [25]. The 2 BC types should receive distinct excitatory input, e.g., from local collaterals of PNs to fulfill independent operations
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