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

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.

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.