Complementary contributions of spike timing and spike rate to perceptual decisions in rat S1 and S2 cortex

Abstract

When a neuron responds to a sensory stimulus, two fundamental codes [1-6] may transmit the information specifying stimulus identity--spike rate (the total number of spikes in the sequence, normalized by time) and spike timing (the detailed millisecond-scale temporal structure of the response). To assess the functional significance of these codes, we recorded neuronal responses in primary (S1) and secondary (S2) somatosensory cortex of five rats as they used their whiskers to identify textured surfaces. From the spike trains evoked during whisker contact with the texture, we computed the information that rate and timing codes carried about texture identity and about the rat's choice. S1 and S2 spike timing carried more information about stimulus and about choice than spike rates; the conjunction of rate and timing carried more information than either code alone. Moreover, on trials when our spike-timing-decoding algorithm extracted faithful texture information, the rat was more likely to choose correctly; when our spike-timing-decoding algorithm extracted misleading texture information, the rat was more likely to err. For spike rate information, the relationship between faithfulness of the message and correct choice was significant but weaker. These results indicate that spike timing makes crucial contributions to tactile perception, complementing and surpassing those made by rate. The language by which somatosensory cortical neurons transmit information, and the readout mechanism used to produce behavior, appears to rely on multiplexed signals from spike rate and timing.