Information about contact force and surface texture is mixed in the firing rates of cutaneous afferent neurons

J Neurophysiol. 2021 Feb 1;125(2):496-508. doi: 10.1152/jn.00725.2019. Epub 2020 Dec 16.

Abstract

Cutaneous mechanoreceptors in our hands gather information about the objects we handle. Tactile fibers encode mixed information about contact events and object properties. Neural coding in tactile afferents is typically studied by varying a single aspect of tactile stimuli, avoiding the confounds of real-world haptic interactions. We instead record responses of small populations of dorsal root ganglia (DRG) neurons to variable tactile stimuli and find that neurons primarily respond to force, though some texture information can be detected. Tactile nerve fibers convey information about many features of haptic interactions, including the force and speed of contact, as well as the texture and shape of the objects being handled. How we perceive these object features is relatively unaffected by the forces and movements we use when interacting with the object. Because signals related to contact events and object properties are mixed in the responses of tactile fibers, our ability to disentangle these different components of our tactile experience implies that they are demultiplexed as they propagate along the neuraxis. To understand how texture and contact mechanics are encoded together by tactile fibers, we studied the activity of multiple neurons recorded simultaneously in the cervical DRG of two anesthetized rhesus monkeys while textured surfaces were applied to the glabrous skin of the fingers and palm using a handheld probe. A transducer at the tip of the textured probe measured contact forces as tactile stimuli were applied at different locations on the finger-pads and palm. We examined how a sample population of DRG neurons encode force and texture and found that firing rates of individual neurons are modulated by both force and texture. In particular, slowly adapting (SA) neurons were more responsive to force than texture, and rapidly adapting (RA) neurons were more responsive to texture than force. Although force could be decoded accurately throughout the entire contact interval, texture signals were most salient during onset and offset phases of the contact interval.NEW & NOTEWORTHY Cutaneous mechanoreceptors in our hands gather information about the objects we handle. Tactile fibers encode mixed information about contact events and object properties. Neural coding in tactile afferents is typically studied by varying a single aspect of tactile stimuli, avoiding the confounds of real-world haptic interactions. We instead record responses of small populations of DRG neurons to variable tactile stimuli and find that neurons primarily respond to force, though some texture information can be detected.

Keywords: cutaneous; dorsal root ganglia; mechanoreceptor; nonhuman primate; sensory.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials*
  • Adaptation, Physiological
  • Animals
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / physiology
  • Macaca mulatta
  • Male
  • Mechanoreceptors / physiology*
  • Skin / cytology
  • Skin / innervation
  • Touch
  • Touch Perception*