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

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. Key words: awake monkeys; primary somatosensory cortex; secondary somatosensory cortex; neural coding; flutter; discrimination; periodicity; mutual informationThe sensation of flutter is produced when mechanical vibrations between 5 and 50 Hz are applied to the skin (Mountcastle et al., 1967;Talbot et al., 1968). Earlier studies using vibrotactile stimuli reported four basic observations: (1) that sensation in the flutter range is mediated by primary afferent fibers and S1 neurons with rapidly adapting properties associated with Meissner's mechanoreceptors (Mountcastle et al., 1967;Talbot et al., 1968); (2) that these afferents and cortical neurons are driven very effectively by periodic flutter stimuli, which evoke highly periodic spike trains (Mountcastle et al., 1969(Mountcastle et al., , 1990Recanzone et al., 1992); (3) that psychophysical performance in frequency discrimination, which is similar for humans and monkeys (LaMotte and Mountcastle, 1975), correlates closely with the discriminability of the evoked, periodic interspike intervals (Mountcastle et al., 1969, Recanzone et al., 1992; and (4) that in afferent and S1 units, the firing rate, computed over hundreds of milliseconds, changes little within the flutter range (Talbot et al., 1968;Mountcastle et al., 1969Mountcastle et al., , 1990Recanzon...

Auditory perceptual decision-making based on semantic categorization of environmental sounds

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Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models

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