High-resolution imaging of skin deformation shows that afferents from human fingertips signal slip onset

Elife. 2021 Apr 22:10:e64679. doi: 10.7554/eLife.64679.

Abstract

Human tactile afferents provide essential feedback for grasp stability during dexterous object manipulation. Interacting forces between an object and the fingers induce slip events that are thought to provide information about grasp stability. To gain insight into this phenomenon, we made a transparent surface slip against a fixed fingerpad while monitoring skin deformation at the contact. Using microneurography, we simultaneously recorded the activity of single tactile afferents innervating the fingertips. This unique combination allowed us to describe how afferents respond to slip events and to relate their responses to surface deformations taking place inside their receptive fields. We found that all afferents were sensitive to slip events, but fast-adapting type I (FA-I) afferents in particular faithfully encoded compressive strain rates resulting from those slips. Given the high density of FA-I afferents in fingerpads, they are well suited to detect incipient slips and to provide essential information for the control of grip force during manipulation.

Keywords: afferent; human; microneurography; neuroscience; skin; tactile; touch.

Plain language summary

Each fingertip hosts thousands of nerve fibers that allow us to handle objects with great dexterity. These fibers relay the amount of friction between the skin and the item, and the brain uses this sensory feedback to adjust the grip as necessary. Yet, exactly how tactile nerve fibers encode information about friction remains largely unknown. Previous research has suggested that friction might not be recorded per se in nerve signals to the brain. Instead, fibers in the finger pad might be responding to localized ‘partial slips’ that indicate an impending loss of grip. Indeed, when lifting an object, fingertips are loaded with a tangential force that puts strain on the skin, resulting in subtle local deformations. Nerve fibers might be able to detect these skin changes, prompting the brain to adjust an insecure grip before entirely losing grasp of an object. However, technical challenges have made studying the way tactile nerve fibers respond to slippage and skin strain difficult. For the first time, Delhaye et al. have now investigated how these fibers respond to and encode information about the strain placed on fingertips as they are loaded tangentially. A custom-made imaging apparatus was paired with standard electrodes to record the activity of four different kinds of tactile nerve fibers in participants who had a fingertip placed against a plate of glass. The imaging focused on revealing changes in skin surface as tangential force was applied; the electrodes measured impulses from individual nerve fibers from the fingertip. While all the fibers responded during partial slips, fast-adapting type 1 nerves generated strong responses that signal a local loss of grip. Recordings showed that these fibers consistently encoded changes in the skin strain patterns, and were more sensitive to skin compressions related to slippage than to stretch. These results show how tactile nerve fibers encode the subtle skin compressions created when fingers handle objects. The methods developed by Delhaye et al. could further be used to explore the response properties of tactile nerve fibers, sensory feedback and grip.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Action Potentials
  • Female
  • Fingers / innervation*
  • Friction
  • Hand Strength*
  • Humans
  • Male
  • Mechanoreceptors / physiology*
  • Mechanotransduction, Cellular*
  • Reaction Time
  • Skin / innervation*
  • Stress, Mechanical
  • Time Factors
  • Touch
  • Touch Perception
  • Young Adult

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.