Dynamic recruitment of PV interneurons in the somatosensory cortex induced by experience dependent plasticity

Abstract

Adaptive circuit plasticity plays crucial roles in the brain during development, learning, sensory experience, and after injury. During chronic whisker trimming, a well-studied paradigm for inducing experience-dependent plasticity, whisker representations in the somatosensory barrel cortex (S1BF) undergo remapping, with expansion of maps for spared whiskers and contraction of maps for trimmed whiskers. At the cellular level, excitatory pyramidal (Pyr) cells in Layer 2/3 shift their whisker tuning, increasing selectivity to spared whiskers and away from deprived whiskers. While these changes are well documented, the circuit mechanisms regulating experience-dependent plasticity remain incompletely characterized. Parvalbumin (PV) interneurons play important roles in regulating the spatial and temporal dynamics of sensory evoked activity in Pyr cells and have been implicated in the regulation of experience-dependent plasticity in other cortical regions. However, there is little evidence as to how the sensory evoked activity of PV cells changes in S1BF during whisker trimming or how those changes might affect cortical remapping. To address these questions, we used longitudinal in vivo two-photon (2P) calcium imaging of PV cells in S1BF before, during, and after inducing experience-dependent plasticity by whisker trimming. At baseline, we found that PV cells have spatially distributed responses to whisker deflections, responding best to the principal whisker of a given barrel and less frequently to surrounding whiskers in a distance-dependent manner. After whisker trimming, there is a substantial recruitment of PV cells responsive to the spared whisker in deprived, but not spared, barrels. Upon whisker regrowth, this recruitment is reversed, but changes in individual PV cell whisker selectivity can persist for weeks. To better understand how changes in PV activity might affect sensory-evoked responses in S1BF, we used chemogenetics to acutely manipulate the activity of PV cells and found that modulating PV cell activity strongly affects sensory-evoked responses in local Pyr and PV cells, as well as Somatostatin (SST) interneurons. Surprisingly, activating PV cell activity strongly suppressed sensory-evoked activity in all three cell types. Computational modeling of the effects of chemogenetic perturbation of PV cells reproduced observed effects on the S1BF microcircuit, underscoring that directly perturbing interneurons in one direction can paradoxically change their activity in the opposite direction due to network effects. Together, our results reveal dynamic changes in the spatial distribution and tuning of PV cells during experience-dependent plasticity and demonstrate that increased PV cell activity can profoundly alter microcircuit dynamics in the adult S1BF.