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.

Short Time-Scale Sensory Coding in S1 during Discrimination of Whisker Vibrotactile Sequences

“…Integration is also implicated in discrimination of surface texture (roughness), in which surface whisking generates temporally dense sequences of stick-slip whisker micromotions, whose mean statistics, including mean whisker speed, correlate with roughness [3,4,21,30–33]. S1 neurons spike phasically to stick/slip events and other features such as dynamic changes in whisker bend [3,21,34], and behavioral judgments of surface roughness correlate with mean firing rate and rate of synchronous spiking across S1 neurons [21,35,36]. Thus, roughness discrimination likely involves temporal integration of stick/slip events and S1 spike trains.…”

Sensory and decision-related activity propagate in a cortical feedback loop during touch perception

“…Anatomy 19,20 and physiology in anesthetized/narcotized rodents 21–23 suggest that mouse S2 is a higher, or more integrative, cortical area compared with S1. However, responses of rodent S2 neurons during tactile behavior are nearly entirely unexplored (but see: 24,25 ). We thus began by mapping responses to stimulation of a single whisker across whisker representation areas of S1 and S2, in separate mice, as they performed the detection task.…”

“…Neurons in both S1 and S2 propagated stimulus- and choice-related activity to the other area. However, neurons in each area also showed key differences in their response properties (see also: 24,25 ). S2 activity was more associated with perceptual outcome compared with S1, whereas S1 activity better encoded the stimulus.…”

Noisy Juxtacellular StimulationIn VivoLeads to Reliable Spiking and Reveals High-Frequency Coding in Single Neurons

“…Information transmission in the brain presumably does not rely exclusively on a summed population activity, but rather is also mediated by the precise spike times of individual cells (Strong et al, 1998;Zuo et al, 2015). Measuring and modeling the singleneuron response to time-dependent stimuli thus remains a crucial task in understanding the neural code (Rieke et al, 1996).…”