Synaptic Mechanisms Underlying Sparse Coding of Active Touch

Sensory information is actively gathered by animals, but the synaptic mechanisms driving neuronal circuit function during active sensory processing are poorly understood. Here, we investigated the synaptically driven membrane potential dynamics during active whisker sensation using whole-cell recordings from layer 2/3 pyramidal neurons in the primary somatosensory barrel cortex of behaving mice. Although whisker contact with an object evoked rapid depolarization in all neurons, these touch responses only drove action potentials in similar to 10% of the cells. Such sparse coding was ensured by cell-specific reversal potentials of the touch-evoked response that were hyperpolarized relative to action potential threshold for most neurons. Intercontact interval profoundly influenced touch-evoked postsynaptic potentials, interestingly without affecting the peak membrane potential of the touch response. Dual whole-cell recordings indicated highly correlated membrane potential dynamics during active touch. Sparse action potential firing within synchronized cortical layer 2/3 microcircuits therefore appears to robustly signal each active touch response.