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

Abstract

The established view is that vibrotactile stimuli evoke two qualitatively distinctive cutaneous sensations, flutter (frequencies < 60 Hz) and vibratory hum (frequencies > 60 Hz), subserved by two distinct receptor types (Meissner's and Pacinian corpuscle, respectively), which may engage different neural processing pathways or channels and fulfil quite different biological roles. In psychological and physiological literature, those two systems have been labelled as Pacinian and non-Pacinian channels. However, we present evidence that low-frequency spike trains in Pacinian afferents can readily induce a vibratory percept with the same low frequency attributes as sinusoidal stimuli of the same frequency, thus demonstrating a universal frequency decoding system. We achieved this using brief low-amplitude pulsatile mechanical stimuli to selectively activate Pacinian afferents. This indicates that spiking pattern, regardless of receptor type, determines vibrotactile frequency perception. This mechanism may underlie the constancy of vibrotactile frequency perception across different skin regions innervated by distinct afferent types.

Keywords: Pacinian afferents; haptics; human; neuroscience; pitch; spike timing; tactile; vibrotactile.

Figure 1.. Detection thresholds.

(A) Vibrotactile detection thresholds on the finger across frequency ranges for sinusoidal and pulsatile stimuli (n = 12). Shaded area represent ± 95% confidence intervals. (B) An example of the sinusoidal and pulsatile waveforms.

Figure 2.. Point of subjective equality (PSE) obtained using two interval forced choice paradigm.

The test stimulus was either sinusoidal or pulsatile presented at 20 Hz and 40 Hz. The test stimulus was compared with a range of comparison frequencies: 10, 14, 18, 22, 26, 30 Hz with 20 Hz test stimulus; and 25, 31, 37, 43, 49, 55 Hz with 40 Hz test stimulus. Black horizontal lines represent mean ± 95% confidence intervals (n = 12).

Figure 2—figure supplement 1.. Insensitivity of frequency rating to changes in stimulus amplitude.

Results are shown for five subjects (n = 5), who conducted the same experimental protocol illustrated in Figures 2 and 3 at 40 Hz, but with two different amplitudes (randomly interleaved) for the comparison frequencies. For the sinusoidal comparisons, the standard was 60 µm, and the comparisons were 40 µm (sine low) and 90 µm (sine high). For the pulsatile comparisons, the standard was 6 µm, and the comparisons were 3 µm (pulse low) and 10 µm (pulse high). Mean values for PSE and Weber fraction for each condition with 95% CI were: [Table: see text]

Figure 3.. The Weber's fraction of just noticeable difference in frequency.

For details refer to legend of Figure 2.

Figure 4.. Experimental protocols.

(A) Structure of the detection threshold task. (B) Structure of the frequency perception task. (C) Point of subjective equality (PSE) determined on the psychometric curve.

Figure 5.. Afferent responses with 20 Hz stimuli.

(A) FAII afferent response to pulsatile stimuli 3 µm in amplitude. (B) FAI afferent response to sinusoidal stimuli 150 µm in amplitude. (C–D) The same FAI afferent as in B, response to pulsatile stimuli at various amplitudes: no response with 25 µm (subthreshold) stimulus; sporadic firing at 30 µm; and entrainment at 35 µm. Note that firing pattern in A, B and E is identical regardless of stimulus or afferent type.