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Shankar Sachidhanandam

Parvalbumin-expressing GABAergic neurons gate sensory perception in mouse barrel cortex

Shankar Sachidhanandam (Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne)

Sensory percepts are thought to be generated by the activity of neurons in the cerebral cortex. However, a causal description of the synaptic interactions driving the neural circuit computations underlying any learned, goal-directed sensorimotor transformation is currently lacking. Here, we explore the role of primary sensory cortex in the simplest possible perceptual task, stimulus detection. Mice were trained to detect single brief whisker stimuli and to report perceived stimuli by licking to obtain a reward. Optogenetic stimulation of the primary somatosensory barrel cortex readily substituted for whisker stimulation in both learning and execution of the detection task. Pharmacological inactivation of barrel cortex prevented detection. The barrel cortex therefore plays a causal role in this behavior. Whole-cell membrane potential recordings from layer 2/3 barrel cortex neurons during task performance revealed that both synchronized, slow oscillatory brain states and desynchronized brain states were compatible with high performance. Whisker deflection evoked an early reliable sensory response, indifferent to behavioral outcome, encoded through cell-specific reversal potentials and sparse reliable action potential firing in excitatory neurons. A secondary late depolarization accompanied by spiking in excitatory neurons was enhanced on hit trials compared to misses. Optogenetic stimulation of parvalbumin-expressing (PV) GABAergic neurons was used to inactivate the barrel cortex with high temporal precision, revealing a causal role for late excitation in the detection task. The late depolarization was likely driven by reduced action potential firing of PV neurons on hit trials. Our data reveal dynamic stimulus processing in sensory cortex during task performance, with an early sensory response reliably encoding the stimulus and later secondary activity contributing to driving the subjective percept as reported through licking.