Compartmental organization of synaptic inputs to parvalbumin-expressing GABAergic neurons in mouse primary somatosensory cortex

Abstract

Parvalbumin (PV)-positive fast-spiking cells in the neocortex are known to generate gamma oscillations by mutual chemical and electrical connections. Recent findings suggest that this rhythm might be responsible for higher-order brain functions, and related to psychiatric disorders. To elucidate the precise structural rules of the connections of PV neurons, we first produced genetic tools. Using a lentiviral expression system, we developed neuron-specific promoters and a new reporter protein that labels the somatodendritic membrane of neurons. We applied the reporter protein to the generation of transgenic mice, and succeeded in visualizing the dendrites and cell bodies of PV neurons efficiently. Then we analyzed excitatory and inhibitory inputs to PV neurons in the primary somatosensory cortex using the mice. Corticocortical glutamatergic inputs were more frequently found on the distal dendrites than on the soma, whereas thalamocortical inputs did not differ between the proximal and distal portions. Corticocortical inhibitory inputs were more densely distributed on the soma than on the dendrites. We further investigated which types of neocortical GABAergic neurons preferred the PV soma over their dendrites. We revealed that the somatic and dendritic compartments principally received GABAergic inputs from vasoactive intestinal polypeptide (VIP)-positive and PV neurons, respectively. This compartmental organization suggests that PV neurons communicate with each other mainly via the dendrites, and that their activity is effectively controlled by the somatic inputs of VIP neurons. These findings provide new insights into the neuronal circuits involving PV neurons, and contribute to a better understanding of brain functions and mental disorders.