Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli

TLDR

Flutter sensation occurs with skin vibrations between 5 and 50 Hz; rapidly adapting somatosensory neurons fire periodic spike trains with regular inter‑spike intervals; it has been conjectured that these periodic patterns encode stimulus frequency rather than mean firing rate. The study examined whether firing rate and spike train periodicity encode vibrotactile frequency by recording extracellular activity in S1 and S2 of awake monkeys during a frequency discrimination task. The authors quantified stimulus‑driven modulations in firing rate and spike train periodicity from the recordings to assess their relevance for frequency discrimination. Periodic spike trains were prominent in S1 but nearly absent in S2, and were enhanced by behaviorally relevant stimuli, yet did not correlate with psychophysical performance; in contrast, firing‑rate modulations were similar across areas, increased with task relevance, and significantly correlated with performance, indicating that firing rate is an important component of the neural code for flutter frequency.

Abstract

The flutter sensation is felt when mechanical vibrations between 5 and 50 Hz are applied to the skin. Neurons with rapidly adapting properties in the somatosensory system of primates are driven very effectively by periodic flutter stimuli; their evoked spike trains typically have a periodic structure with highly regular time differences between spikes. A long-standing conjecture is that, such periodic structure may underlie a subject's capacity to discriminate the frequencies of periodic vibrotactile stimuli and that, in primary somatosensory areas, stimulus frequency is encoded by the regular time intervals between evoked spikes, not by the mean rate at which these are fired. We examined this hypothesis by analyzing extracellular recordings from primary (S1) and secondary (S2) somatosensory cortices of awake monkeys performing a frequency discrimination task. We quantified stimulus-driven modulations in firing rate and in spike train periodicity, seeking to determine their relevance for frequency discrimination. We found that periodicity was extremely high in S1 but almost absent in S2. We also found that periodicity was enhanced when the stimuli were relevant for behavior. However, periodicity did not covary with psychophysical performance in single trials. On the other hand, rate modulations were similar in both areas, and with periodic and aperiodic stimuli, they were enhanced when stimuli were important for behavior, and were significantly correlated with psychophysical performance in single trials. Thus, the exquisitely timed, stimulus-driven spikes of primary somatosensory neurons may or may not contribute to the neural code for flutter frequency, but firing rate seems to be an important component of it.