Slowly-adapting type II afferents contribute to conscious touch sensation in humans: Evidence from single unit intraneural microstimulation

Abstract

Slowly-adapting type II (SA-II, Ruffini) mechanoreceptive afferents respond well to pressure and stretch, and are regularly encountered in human microneurography studies. Despite an understanding of SA-II response properties, their role in touch perception remains unclear. Specific roles of different myelinated Aβ mechanoreceptive afferents in tactile perception have been revealed using single unit intraneural microstimulation (INMS), via microneurography, recording from and then electrically stimulating individual afferents. This method directly links single afferent artificial activation to perception, where INMS produces specific 'quantal' touch percepts associated with different mechanoreceptive afferent types. However, SA-II afferent stimulation has been ambiguous, producing inconsistent, vague sensations, or no clear percept. We physiologically characterized hundreds of individual Aβ mechanoreceptive afferents in the glabrous hand skin and examined the subsequent percepts evoked by trains of low amplitude INMS current pulses (<10 μA). We present 18 SA-II afferents where INMS resulted in a clear, electrically evoked sensation of large (∼36 mm² ) diffuse pressure, which was projected precisely to their physiologically-defined receptive field in the skin. This sensation was felt as natural, distinctive from other afferents, and showed no indications of multi-afferent stimulation. Stimulus frequency modulated sensation intensity and even brief stimuli (4 pulses, 60 ms) were perceived. These results suggest that SA-II afferents contribute to perceived tactile sensations, can signal this rapidly and precisely, and are relevant and important for computational models of touch sensation and artificial prosthetic feedback. KEY POINTS: Slowly adapting type II mechanoreceptors (SA-IIs) are primary sensory neurons in humans that respond to pressure and stretch applied to the skin. To date, no specific conscious correlate of touch has been linked to SA-II activation. Using microneurography and intraneural microstimulation to stimulate single sensory neurons in human subjects, we find a specific sensation linked to the activation of single SA-II afferents. This sensation of touch was reported as gentle pressure and subjects could detect this with a high degree of accuracy. Methods of artificial tactile sensory feedback and computational models of touch should include SA-IIs as meaningful contributors to the conscious sensation of touch.

Keywords: Ruffini; SA-II; mechanoreceptor; pressure; skin; tactile; touch.