In rodent whisker sensation, whisker position signals, including whisking phase, are integrated with touch signals to enable spatially accurate tactile perception, but other functions of phase coding are unclear. We investigate how phase coding affects the neural coding of surface features during surface whisking. In mice performing rough-smooth discrimination, S1 units exhibit much stronger phase tuning during surface whisking than in prior studies of whisking in air. Among putative pyramidal cells, preferred phase tiles phase space, but protraction phases are strongly over-represented. Fast-spiking units are nearly all protraction tuned. This protraction bias increases the coding of stick-slip whisker events during protraction, suggesting that surface features are preferentially encoded during protraction. Correspondingly, protraction-tuned units encode rough-smooth texture better than retraction-tuned units and encode the precise spatial location of surface ridges with higher acuity. This suggests that protraction is the main information-gathering phase for high-resolution surface features, with phase coding organized to support this function.

Tactile objects have both local geometry (shape) and broader macroscopic texture, but how these different spatial scales are simultaneously encoded during active touch is unknown. In the whisker system, we tested for a shared code based on localized whisker micromotions (stick-slips) and slip-evoked spikes. We trained mice to discriminate smooth from rough surfaces, including ridged gratings and sandpaper. Whisker slips locked to ridges and evoked temporally precise spikes (<10 ms jitter) in somatosensory cortex (S1) that could resolve ridges with ∼1 mm accuracy. Slip-sensitive neurons also encoded touch and texture. On rough surfaces, both slip-evoked spikes and an additional non-slip signal elevated mean firing rate, allowing accurate rough-smooth texture decoding from population firing rate. Eighteen percent of neurons were selective among rough surfaces. Thus, slips elicit spatially and temporally precise spiking in S1 that simultaneously encodes local shape (ridges) and is integrated into a macroscopic firing rate code for roughness.

Local recurrent networks in neocortex are critical nodes for sensory processing, but their regulation by experience is much less understood than for long-distance (translaminar or cross-columnar) projections. We studied local L2/3 recurrent networks in rat somatosensory cortex during deprivation-induced whisker map plasticity, by expressing channelrhodopsin-2 (ChR2) in L2/3 pyramidal cells and measuring light-evoked synaptic currents in ex vivo S1 slices. In columns with intact whiskers, brief light impulses evoked recurrent excitation and supralinear inhibition. Deprived columns showed modestly reduced excitation and profoundly reduced inhibition, providing a circuit locus for disinhibition of whisker-evoked responses observed in L2/3 in vivo. Slower light ramps elicited sustained gamma frequency oscillations, which were nearly abolished in deprived columns. Reduction in gamma power was also observed in spontaneous LFP oscillations in L2/3 of deprived columns in vivo. Thus, L2/3 recurrent networks are a powerful site for homeostatic modulation of excitation-inhibition balance and regulation of gamma oscillations.