Multiplexing Stimulus Information through Rate and Temporal Codes in Primate Somatosensory Cortex

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Abstract
Our ability to perceive and discriminate textures relies on the transduction and processing of complex, high-frequency vibrations elicited in the fingertip as it is scanned across a surface. How naturalistic vibrations, and by extension texture, are encoded in the responses of neurons in primary somatosensory cortex (S1) is unknown. Combining single unit recordings in awake macaques and perceptual judgments obtained from human subjects, we show that vibratory amplitude is encoded in the strength of the response evoked in S1 neurons. In contrast, the frequency composition of the vibrations, up to 800 Hz, is not encoded in neuronal firing rates, but rather in the phase-locked responses of a subpopulation of neurons. Moreover, analysis of perceptual judgments suggests that spike timing not only conveys stimulus information but also shapes tactile perception. We conclude that information about the amplitude and frequency of natural vibrations is multiplexed at different time scales in S1, and encoded in the rate and temporal patterning of the response, respectively. When we slide our fingertip across a textured surface, small, complex, and high-frequency vibrations are elicited in the skin and our nervous system extracts information about texture from these vibrations. In this study, we investigate how texture-like vibrations are processed in primary somatosensory cortex (S1). First, we show that the time-varying amplitude of skin vibrations is encoded in the time-varying response rates of a subpopulation of S1 neurons. Second, we show that this same subpopulation of S1 neurons produces responses whose timing closely matches that of the vibrations: The frequency composition of the spiking patterns matches that of the stimulus, even for complex vibrations. We demonstrate that this temporal precision is behaviorally relevant by showing that the tactile perception of vibration is better predicted from neuronal responses when spike timing is taken into consideration than when it is not. The activity of S1 neurons is thus multiplexed at different time scales: Stimulus amplitude, which changes relatively slowly, is represented at a relatively coarse temporal resolution, while stimulus frequency is represented by precisely timed action potentials.