Millisecond precision temporal encoding of stimulus features during cortically generated gamma oscillations in the rat somatosensory cortex.

KEY POINTS: Rodents explore their immediate environment using their whiskers. Such exploration leads to micromotions, which contain many high-frequency (50-200 Hz) components. High-frequency whisker motion is represented faithfully in the temporal structure of the spike trains of trigeminal neurons. However, the representation of high-frequency sensory inputs in cortex is not fully understood. By combining extracellular and intracellular recordings in the rat somatosensory cortex and thalamus, we show that high-frequency sensory inputs, either sinusoidal or white noise, elicit internally generated gamma (20-60 Hz) band oscillations in cortical networks. Gamma oscillations modulate cortical spike probability while preserving sub-millisecond phase relations with high-frequency sensory inputs. Consequently, our results indicate that millisecond precision stimulus-locked spiking activity and sensory-induced gamma oscillation can constitute independent multiplexed coding schemes at the single-cell level. ABSTRACT: In the natural environment, tactile exploration often leads to high-frequency vibrations at the level of the sensory organs. Single-unit recordings of cortical neurons have pointed towards either a rate or a temporal code for representing high-frequency tactile signals. In cortical networks, sensory processing results from the interaction between feedforward inputs relayed from the thalamus and internally generated activity. However, how the emergent activity represents high-frequency sensory input is not fully understood. Using multisite single-unit, local field potential and intracellular recordings in the somatosensory cortex and thalamus of lightly sedated male rats, we measured neuronal responses evoked by sinusoidal and band-pass white noise whisker stimulation at frequencies that encompass those observed during texture exploration (50-200 Hz). We found that high-frequency sensory inputs relayed from the thalamus elicit both sub-millisecond stimulus-locked responses and internally generated gamma (20-60 Hz) band oscillations in cortical networks. Gamma oscillations modulate spike probability while preserving sub-millisecond phase relations with sensory inputs. Therefore, precise stimulus-locked spiking activity and sensory-induced gamma oscillations can constitute independent multiplexed coding schemes at the single-cell level.