Diverse tuning underlies sparse activity in layer 2/3 vibrissal cortex of awake mice

Key points: Sparse population activity is a common feature observed across cortical areas, yet the implications for sensory coding are not clear. We recorded single neuron activity in the vibrissal somatosensory cortex of awake head-fixed mice using the cell-attached technique. Unlike the anaesthetised condition, in awake mice a high-velocity, piezo-controlled whisker deflection excited only a small fraction of neurons. Manual probing of whiskers revealed that the majority of these silent neurons could be activated by specific forms of whisker–object contact. Our results suggest that sparse coding in vibrissal cortex may be due to high dimensionality of the stimulus space and narrow tuning of individual neurons. Abstract: It is widely reported that superficial layers of the somatosensory cortex exhibit sparse firing. This sparseness could reflect weak feedforward sensory inputs that are not sufficient to generate action potentials in these layers. Alternatively, sparseness might reflect tuning to unknown or higher-level complex features that are not fully explored in the stimulus space. Here, we examined these hypotheses by applying a range of vibrotactile and manual vibrissal stimuli in awake, head-fixed mice while performing loose-seal cell-attached recordings from the vibrissal primary somatosensory (vS1) cortex. A high-velocity stimulus delivered by a piezo-electric actuator evoked activity in a small fraction of regular spiking supragranular neurons (23%) in the awake condition. However, a majority of the supragranular regular spiking neurons (84%) were driven by manual stimulation of whiskers. Our results suggest that most neurons in the superficial layers of vS1 cortex contribute to coding in the awake condition when neurons may encounter their preferred feature(s) during whisker–object interactions.