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Perceived tactile intensity at a fixed primary afferent spike rate varies with the temporal pattern of spikes.

Deepak SharmaKevin K W NgIngvars BirznieksRichard M Vickery
Published in: Journal of neurophysiology (2022)
The perceived intensity of a vibrotactile stimulus is thought to depend on single-neuron firing rates (rate coding) and the number of active afferents (population coding). Unaddressed until now is whether the temporal relation of individual spikes also conveys information about tactile intensity. We used cutaneous electro-tactile stimulation to investigate how the temporal structure of a fixed number of spikes in a 1-s train influenced the perception of intensity. Four mean spike rates spanning the flutter and vibratory hum range (36 Hz, 60 Hz; 120 Hz, 180 Hz) were tested, with spikes grouped into a regular pattern, or bursts of 2-6 spikes spaced 3 ms apart. To link a putative neural code to perception, perceived intensity was assessed in 16 human participants (aged 20-45; 4 females) using the psychophysical paradigm of magnitude estimation. Compound sensory nerve action potentials were recorded to assess any stimulus variation in afferent recruitment. The temporal structuring of a fixed number of spikes into periodic bursts of multiple spikes altered perceived intensity as a function of burst spike count. The largest increase was seen at 36 Hz, where the bursts of six spikes were rated 2.1 times stronger than the regularly spaced spikes [95% confidence interval (CI): 1.9-2.3]. The true increase is likely larger as temporal structuring of spikes into bursts had some negative effect on afferent recruitment. We conclude that the perceived intensity can be modulated by changing temporal features of afferent discharge even when normalized for the number of recruited afferents.<b>NEW &amp; NOTEWORTHY</b> Structuring a fixed number of spikes into temporal burst patterns evoke gradations of perceived intensity with burst spike count, emphasizing the importance of spike timing in primary afferents for shaping perception. This forms the basis for new strategies in communicating a range of intensity information to users of neural interfaces by simply varying the timing of spikes in nonspecific primary afferents using fixed-charge electric pulses, without requiring alterations in stimulation current or mean pulse frequency.
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