Electrotactile frequency perception over multiple stimulation sites does not use a winner-takes-all mechanism

It is not known how the brain extracts vibrotactile stimulus frequency from the peripheral afferent population whose afferents exhibit a wide range of response patterns to a pure frequency stimulus, including afferents which do not respond to every vibration cycle of the stimulus and thus have lower firing rates. One hypothesis is a winner-takes-all mechanism based on the peripheral afferents with the highest or most regular firing rate, which discounts those firing at lower rates. We used a high-resolution fingertip electrode array and activated some electrodes at 40 Hz and others at 20 Hz to investigate integration of tactile afferent population input signalling frequency information. Participants (n = 12) gave ratings of frequency for these mixed-frequency stimuli against a standard pure frequency. Participants reported perceiving a unified holistic frequency for the mixed-frequency stimuli. This perceived frequency did not match any inter-pulse intervals in the stimulus; instead, it appeared to represent a weighted measure of the two presented frequencies. Our findings add to previous reports of frequency averaging for multiple mechanical stimuli, which suggest that activity across the whole population of activated afferents determines frequency perception. That frequency perception may be based on weighted averaging across all afferents has implications for applications of electrical nerve stimulation for sensory feedback. KEY POINTS: Vibration of the skin causes a wide range of response patterns in tactile afferents of the responding neural population. It has been proposed that a winner-takes-all mechanism favouring afferents with the highest or most regular firing rate enables the nervous system to extract the vibration frequency of the applied stimulus. We stimulated fingertip tactile afferents via an electrical array, with a variable proportion of electrodes activated at 40 Hz and the rest at 20 Hz, and asked participants to make judgements about the stimulus frequency. The perceived frequency was not locked to the highest presented frequency, but instead increased gradually in all participants as the proportion of electrodes delivering 40 Hz increased. This shows that a winner-takes-all mechanism does not operate; instead, the entire population of responding afferents contribute with some weighting factor to vibration frequency perception.