Tactile sensory channels over-ruled by frequency decoding system that utilizes spike pattern regardless of receptor type

Abstract

2The established view is that vibrotactile stimuli evoke two qualitatively distinctive cutaneous sensations, 3 flutter (frequencies < 60 Hz) and vibratory hum (frequencies > 60 Hz), subserved by two distinct 4 receptor types (Meissner's and Pacinian corpuscle, respectively) which may engage different neural 5 processing pathways or channels and fulfill quite different biological roles. In psychological and 6 physiological literature those two systems have been labelled as Pacinian and non-Pacinian channels. 7However, we present evidence that low-frequency spike trains in Pacinian afferents can readily induce a 8 vibratory percept with the same low frequency attributes as sinusoidal stimuli of the same frequency 9 thus demonstrating a universal frequency decoding system. We achieved this using brief low-amplitude 10 pulsatile mechanical stimuli to selectively activate Pacinian afferents. This indicates that spiking pattern, 11 regardless of receptor type, determines vibrotactile frequency perception. This mechanism may underlie 12 the constancy of vibrotactile frequency perception across different skin regions innervated by distinct 13 afferent types. 14 15 Johansson, 1984). Observations that different receptor types are tuned to different stimulus features and 20 have distinct response profiles have led researchers to conclude that different receptor types are the 21 inputs to separate neural "channels" dedicated to processing of those features (Bolanowski, Gescheider, 22 operating range of one of the channels seems less likely. 132Recent psychophysical evidence demonstrated that there is interaction between the FAI and FAII inputs, 133by showing the assimilation effect, where a frequency in the range of one channel can influence 134 perceived frequency on the other channel (Kuroki, Watanabe, & Nishida, 2017). We suggest that our 135 data extends this, and represents evidence of the functional consequence of the recently discovered 136 extensive convergence of FAI-and FAII-derived inputs onto S1 cortical neurons (Carter, 262The amplitude of all pulsatile stimuli was 3 µm which was approximately 3 times the sensory threshold 263 found in our detection threshold experiment. At this amplitude, we expect only Pacinian (PC) afferents 264 to respond, as threshold for recruitment of FAI afferents, even at their preferred frequency, is no lower

Temporal patterns in electrical nerve stimulation: Burst gap code shapes tactile frequency perception

“…These findings are consistent with recent findings from our laboratory which revealed that the spiking pattern, rather than activated afferent type, determined the perceived frequency of repetitive mechanical stimuli [ 16 ]. In that study, we found that low-frequency spike trains in Pacinian (FA2) afferents could induce a vibratory percept, even though Meissner (FA1) afferents had been traditionally thought to be solely responsible for perception of low frequency flutter vibrations (<60 Hz), whereas higher frequency activation of Pacinian (FA2) afferents would evoke a different percept of vibratory hum [ 24 ].…”

“…While the results in our first experiment, where we used electrical pulses to create bursting trains of the same periodicity but different number of spikes, were best explained by the burst gap code rather than a periodicity or rate code, the mean PSEs were lower than that would be predicted simply from the inter-burst duration. Though the difference in PSEs between electrical and mechanical stimulation was statistically significant, it is unknown whether this difference indicates any physiological importance, as it is well within the Weber fraction of ~0.2–0.3 that has been previously reported in the literature [ 16 , 34 – 38 ]. One possible explanation for this bias towards lower frequencies may be that electrical stimulation recruits all afferent types non-selectively, so that the slowly adapting (SA) afferents would be recruited in addition to the fast adapting (FA) afferents, whereas the mechanical stimulus predominantly activated FA afferents [ 5 ].…”

“…The discovery of the burst gap code for perceived frequency depended on the use of brief mechanical pulses that each only evoke a single spike in responding afferents, as had been verified using microneurography, allowing us to precisely control the spiking pattern of responding tactile afferents [ 5 , 16 , 17 ]. Electrical stimulation activates peripheral axons in a manner different than that of mechanical stimulation [ 18 ], by bypassing the specialised mechanoreceptors in the skin and directly stimulating the tactile afferent axons [ 19 , 20 ].…”

Humans Use a Temporally Local Code for Vibrotactile Perception

“…invariably reaching a discriminability value of 1), a phenomenon consistent with our notion (and with numerous previous studies) that afferents being temporally local encoders (e.g. Birznieks et al, 2019;Gerdjikov et al, 2010;Stüttgen and Schwarz, 2010). A trivial consequence of measuring responses to single pulses, from neurons devoid of spike adaptation, is that increasing pulse frequency does not affect discriminability.…”

A touch of hierarchy: population receptive fields reveal fingertip integration in Brodmann areas in human primary somatosensory cortex

“…Third, the increase in the observed pRF size for higher frequencies of vibrotactile stimulation might be an extra-classical receptive field effect (Friston 2005 ; Schwabe et al 2006 ). It has been suggested that vibrotactile frequency discrimination is not solely driven by mechanoreceptive afferents (Kuroki et al 2017 ; Birznieks et al 2019 ). There may be an additional system for vibrotactile frequency processing, possibly involving horizontal connections (Schwark and Jones 1989 ) or the secondary somatosensory cortex (Nelson et al 2004 ; Chung et al 2013 ; Kalberlah et al 2013 ).…”