Fingertip viscoelasticity enables human tactile neurons to encode loading history alongside current force

Human skin and its underlying tissues constitute a viscoelastic medium, implying that any deformation depends not only on the currently applied force, but also on the recent loading history. The extent to which this physical memory influences the signaling of first-order tactile neurons during natural hand use is not well understood. Here, we examined the effect of past loading on the responses of fast-adapting (FA-1) and slowly-adapting (SA-1 and SA-2) first-order tactile neurons innervating the human fingertip to loadings applied in different directions representative of object manipulation tasks. We found that variation in the preceding loading affected neurons’ overall signaling of force direction. Some neurons kept signaling the current direction, while others signaled both the current and preceding direction, or even primarily the preceding direction. In addition, ongoing impulse activity in SA-2 neurons between loadings signaled information related to the fingertip’s viscoelastic deformation state. We conclude that tactile neurons at the population level signal continuous information about the fingertip’s viscoelastic deformation state, which is shaped by both its recent history and current loading. Such information might be sufficient for the brain to correctly interpret current force loading and help in computing accurate motor commands for interactions with objects in manipulation and haptic tasks.