Spike Timing Matters in Novel Neuronal Code Involved in Vibrotactile Frequency Perception

Abstract

Skin vibrations sensed by tactile receptors contribute significantly to the perception of object properties during tactile exploration [1-4] and to sensorimotor control during object manipulation [5]. Sustained low-frequency skin vibration (<60 Hz) evokes a distinct tactile sensation referred to as flutter whose frequency can be clearly perceived [6]. How afferent spiking activity translates into the perception of frequency is still unknown. Measures based on mean spike rates of neurons in the primary somatosensory cortex are sufficient to explain performance in some frequency discrimination tasks [7-11]; however, there is emerging evidence that stimuli can be distinguished based also on temporal features of neural activity [12, 13]. Our study's advance is to demonstrate that temporal features are fundamental for vibrotactile frequency perception. Pulsatile mechanical stimuli were used to elicit specified temporal spike train patterns in tactile afferents, and subsequently psychophysical methods were employed to characterize human frequency perception. Remarkably, the most salient temporal feature determining vibrotactile frequency was not the underlying periodicity but, rather, the duration of the silent gap between successive bursts of neural activity. This burst gap code for frequency represents a previously unknown form of neural coding in the tactile sensory system, which parallels auditory pitch perception mechanisms based on purely temporal information where longer inter-pulse intervals receive higher perceptual weights than short intervals [14]. Our study also demonstrates that human perception of stimuli can be determined exclusively by temporal features of spike trains independent of the mean spike rate and without contribution from population response factors.

Neural Basis of Touch and Proprioception in Primate Cortex

“…9A). This temporal patterning in afferent responses carries information about the frequency composition of vibratory stimuli applied to the skin (21, 233). …”

Rapid geometric feature signaling in the spiking activity of a complete population of tactile nerve fibers

“…We do not claim there exists no other mechanism that could extract information about geometric features from precise spike timing, for example at the level of populations of nerve fibers through a coincidence detection mechanism (Pruszynski and Johansson, 2014). Neither do we claim that spike timing plays no role in tactile coding, as millisecond level spike-timing of afferent responses has been shown to play a role in the coding of texture (Weber et al, 2013) and of the frequency of skin vibrations (Mackevicius et al, 2012; Birznieks and Vickery, 2017). The present results demonstrate, however, that the classical model of orientation signaling in touch – broadly analogous to its visual counterpart – operates on a time scale that is rapid (and precise) enough to guide object interactions without taking spike timing into account.…”

Emergence of an invariant representation of texture in primate somatosensory cortex

“…In the above analyses, we compare texture representations in afferent firing rates and cortical firing rates. However, a large body of evidence suggests that stimulus information is not encoded simply in the firing rates of tactile nerve fibers, but rather in spatio-temporal patterns of activation (Birznieks and Vickery, 2017;Connor and Johnson, 1992;DiCarlo and Johnson, 2000;LaMotte and Mountcastle, 1975;Mackevicius et al, 2012;Talbot et al, 1968;Weber et al, 2013). These putative peripheral neural codes imply computations along the neuraxis where spatio-temporal motifs in the afferent input are converted to firing rate codes downstream.…”