High-velocity stimulation evokes "dense" population response in layer 2/3 vibrissal cortex

Abstract

Supra-granular layers of sensory cortex are known to exhibit sparse firing. In rodent vibrissal cortex, a small fraction of neurons in layer 2 and 3 (L2/3) respond to whisker stimulation. Here, we combined whole-cell recording and two-photon imaging in anesthetized mice and quantified the synaptic response and spiking profile of L2/3 neurons. Previous literature has shown that neurons across layers of vibrissal cortex are tuned to the velocity of whisker movement. We therefore used a broad range of stimuli that included the standard range of velocities (0-1.2 degree/ms) and extended to a "sharp" high-velocity deflection (3.8 degree/ms). Consistent with previous literature, whole-cell recording revealed a sparse response to the standard range of velocities: although all recorded cells showed tuning to velocity in their postsynaptic potentials, only a small fraction produced stimulus-evoked spikes. In contrast, the sharp stimulus evoked reliable spiking in the majority of neurons. The action-potential threshold of spikes evoked by the sharp stimulus was significantly lower than that of the spontaneous spikes. Juxta-cellular recordings confirmed that application of sharp stimulus to single or multiple whiskers produced temporally precise spiking with minimal trial-to-trial spike-count variability (Fano factors equal or close to the theoretical minimum). Two-photon imaging further confirmed that most neurons that were not responsive to the standard deflections responded to the sharp stimulus. Altogether, our results indicate that sparseness in L2/3 cortex depends on the choice of stimulus: strong single- or multi-whisker stimulation can induce the transition from sparse to "dense" population response.