Parvalbumin-Expressing GABAergic Neurons in Mouse Barrel Cortex Contribute to Gating a Goal-Directed Sensorimotor Transformation

Abstract

SummarySensory processing in neocortex is primarily driven by glutamatergic excitation, which is counterbalanced by GABAergic inhibition, mediated by a diversity of largely local inhibitory interneurons. Here, we trained mice to lick a reward spout in response to whisker deflection, and we recorded from genetically defined GABAergic inhibitory neurons in layer 2/3 of the primary somatosensory barrel cortex. Parvalbumin-expressing (PV), vasoactive intestinal peptide-expressing (VIP), and somatostatin-expressing (SST) neurons displayed distinct action potential firing dynamics during task performance. Whereas SST neurons fired at low rates, both PV and VIP neurons fired at high rates both spontaneously and in response to whisker stimulation. After an initial outcome-invariant early sensory response, PV neurons had lower firing rates in hit trials compared to miss trials. Optogenetic inhibition of PV neurons during this time period enhanced behavioral performance. Hence, PV neuron activity might contribute causally to gating the sensorimotor transformation of a whisker sensory stimulus into licking motor output.

Loss of Mecp2 Causes Atypical Synaptic and Molecular Plasticity of Parvalbumin-Expressing Interneurons Reflecting Rett Syndrome–Like Sensorimotor Defects

“…PV + IN activity regulates high-order processing in the cortex by generating precisely timed inhibition/disinhibition of output target neurons (Zhang and Sun, 2011; Pi et al, 2013). Importantly, the plasticity of PV + IN responses controls the activity of specific neocortical circuits and contributes to sensory and motor information processing during behavioral learning (Cardin et al, 2009; Isomura et al, 2009; Sachidhanandam et al, 2016). For instance, PV + INs in the motor cortex exhibit cellular and molecular plasticity when a mouse learns a novel sensory-motor task, such as the rotarod test.…”

Voltage-sensitive dye imaging of mouse neocortex during a whisker detection task

“…All whiskers were trimmed except for the C2 whiskers on either side. The behavioral training was carried out more or less as previously described, 33,35,36,38 except that (i) in this study, we had an explicit cue from shutter and imaging light indicating trial onset and (ii) unlike in the previous studies, here we did not abort trials with prestimulus licking. Briefly, water-restricted mice were taught to associate a 1-ms magnetic pulse applied to iron particles attached to the right C2 whisker delivered 2.5 s after the trial onset cue with water availability, delivered via a reward spout.…”

“…Here, we imaged neocortical function using VSD during a simple sensorimotor task in which a thirsty mouse converts a single brief whisker-deflection into licking for water reward. Previous investigations of closely related whisker-dependent detection tasks have found task-dependent correlations in action potential firing and membrane potential dynamics of individual neocortical neurons recorded in S1 [33][34][35][36] and M1, 37 as well as in striatal projection neurons. 38 Inactivation of S1 disrupts behavioral performance in whisker-detection tasks, reducing hit rates.…”

Long‐range cortical dynamics: a perspective from the mouse sensorimotor whisker system

“…For L2/3 inhibitory neurons, whisker stimulus drove parvalbumin‐positive (PV+) and VIP+ neurons, whereas SOM+ neurons fired at low rates. PV+ neurons also exhibited choice‐related activity in the period between the early sensory response and when the animal reported their choice, suggesting that this cell type contributes to gating sensorimotor transformation after initial sensory processing (Sachidhanandam et al ., ). Calcium activity in the apical dendrites of L5 pyramidal neurons has also been identified to contribute to the sensory detection threshold during this task (Takahashi et al ., ).…”