Cell-type-specific recruitment of GABAergic interneurons in the primary somatosensory cortex by long-range inputs

Extensive hierarchical yet highly reciprocal interactions among cortical areas are fundamental for information processing. However, connectivity rules governing the specificity of such corticocortical connections, and top-down feedback projections in particular, are poorly understood. We analyze synaptic strength from functionally relevant brain areas to diverse neuronal types in the primary somatosensory cortex (S1). Long-range projections from different areas preferentially engage specific sets of GABAergic neurons in S1. Projections from other somatosensory cortices strongly recruit parvalbumin (PV)-positive GABAergic neurons and lead to PV neuron-mediated feedforward inhibition of pyramidal neurons in S1. In contrast, inputs from whisker-related primary motor cortex are biased to vasoactive intestinal peptide (VIP)-positive GABAergic neurons and potentially result in VIP neuron-mediated disinhibition. Regardless of the input areas, somatostatin-positive neurons receive relatively weak long-range inputs. Computational analyses suggest that a characteristic combination of synaptic inputs to different GABAergic IN types in S1 represents a specific long-range input area. [Display omitted] •Diverse long-range inputs engage distinct GABAergic neurons in S1•S2 inputs recruit PV neurons leading to feedforward inhibition of pyramidal cells in S1•M1 inputs recruit VIP neurons leading to disinhibition of pyramidal cells in S1•SST neurons receive relatively weak long-range inputs regardless of input area Naskar et al. show how functionally relevant brain areas interact with neurons in the primary somatosensory cortex, demonstrating that long-range projections from diverse brain areas differentially recruit specific subtypes of GABAergic neurons in S1, and each distinct subtype of GABAergic neurons differentially affects local network activity in S1.