A Morphologically Distinct Subclass of Somatostatin-expressing Interneurons in the Somatosensory Cortex are Strongly Recruited by Input from the Motor Cortex

Abstract

The motor cortex (M1) and somatosensory cortex (S1) are strongly interconnected regions, and their interactions are essential for sensory perception and motor execution. However, the mechanisms by which M1 activity modulates sensory processing within S1 are poorly understood. In particular, M1 recruitment of distinct GABAergic inhibitory cells could impact S1 responsiveness. Preliminary work in our lab identified a subpopulation of somatostatin (SOM) expressing inhibitory interneurons in layer 6 (L6) of S1 that are strongly recruited by M1 input. We hypothesize these M1-responding L6 SOM cells are an electrophysiological and morphologically distinct subclass that express the enzyme neuronal nitric oxide synthase (nNOS). To stimulate the M1 to S1 pathway and test this hypothesis, we injected adeno-associated virus (AAV) encoding the light-sensitive cation channel, channelrhodopsin-2 (ChR2), in M1 of postnatal day 21 (+/-1) mice in vivo. After three weeks of expression, we prepared acute coronal brain slices for targeted loose-patch recordings and selective optical stimulation of M1 terminals. We found two groups of L6 SOM cells based on their spiking behavior during photostimulation: responsive (15%) and non-responsive (85%). Whole-cell recordings and neurobiotin injections into responsive and non-responsive SOM cells revealed robust electrophysiological and morphological differences. Initial anatomical reconstructions indicate that the non-responsive SOM cells (n=12) exhibit both Martinotti (with an L1 axonal projection) and non-Martinotti (no L1 axonal projection) morphologies, whereas the responsive SOM cells had axonal arborizations projecting toward the underlying white matter (n=10). The responsive SOM cells had quasi-fast-spiking electrophysiological properties (n=10) and were negative for nNOS (n=9), whereas the non-responsive SOM cells exhibited non-adaptive spiking behavior. Importantly, responsive SOM cells were negative for parvalbumin (PV), a marker for a distinct class of fast-spiking interneurons in the cortex, indicating these cells were not mislabeled PV cells due to the known off-target recombination in the SOM-IRES-Cre mouse line (n=4). In summary, our data show that input from M1 strongly recruits a previously unknown SOM-expressing interneuron in lower L6 with distinct morphological and electrophysiological features that could influence sensory responsiveness in S1. Future studies will focus on the mechanisms of this selective activation and identifying the postsynaptic targets of these cells to further our understanding of this sensorimotor circuit. NIH R01NS117636 (SRC); APS SURF (MKS). This is the full abstract presented at the American Physiology Summit 2024 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.