TY - JOUR
T1 - How Tactile Afferents in the Human Fingerpad Encode Tangential Torques Associated with Manipulation
T2 - Are Monkeys Better than Us?
AU - Loutit, Alastair J.
AU - Wheat, Heather E.
AU - Khamis, Heba
AU - Vickery, Richard M.
AU - Macefield, Vaughan G.
AU - Birznieks, Ingvars
N1 - Funding Information:
Received June 23, 2022; revised Apr. 14, 2023; accepted Apr. 17, 2023. Author contributions: H.E.W., V.G.M., and I.B. designed research; V.G.M. and I.B. performed research; H.E.W., H.K., R.M.V., V.G.M., and I.B. contributed unpublished reagents/analytic tools; A.J.L. analyzed data; A.J.L. wrote the first draft of the paper; A.J.L., H.K., R.M.V., V.G.M., and I.B. edited the paper; A.J.L. wrote the paper. This project was funded by the Australian Research Council (ARC). We thank Prof. Antony W Goodwin for contribution to the inception of this study as well designing and providing stimulators from his laboratory. We thank Dr. Rachael Brown for help with spike sorting procedures. *H. E. Wheat is now retired. The authors declare no competing financial interests. Correspondence should be addressed to Alastair J. Loutit at [email protected]. https://doi.org/10.1523/JNEUROSCI.1305-22.2023 Copyright © 2023 the authors
Publisher Copyright:
Copyright © 2023 the authors.
PY - 2023/5/31
Y1 - 2023/5/31
N2 - Dexterous object manipulation depends critically on information about forces normal and tangential to the fingerpads, and also on torque associated with object orientation at grip surfaces. We investigated how torque information is encoded by human tactile afferents in the fingerpads and compared them to 97 afferents recorded in monkeys (n=3; 2 females) in our previous study. Human data included slowly-adapting Type-II (SA-II) afferents, which are absent in the glabrous skin of monkeys. Torques of different magnitudes (3.5-7.5 mNm) were applied in clockwise and anticlockwise directions to a standard central site on the fingerpads of 34 human subjects (19 females). Torques were superimposed on a 2, 3, or 4 N background normal force. Unitary recordings were made from fast-adapting Type-I (FA-I, n=39), and slowly-adapting Type-I (SA-I, n=31) and Type-II (SA-II, n=13) afferents supplying the fingerpads via microelectrodes inserted into the median nerve. All three afferent types encoded torque magnitude and direction, with torque sensitivity being higher with smaller normal forces. SA-I afferent responses to static torque were inferior to dynamic stimuli in humans, while in monkeys the opposite was true. In humans this might be compensated by the addition of sustained SA-II afferent input, and their capacity to increase or decrease firing rates with direction of rotation. We conclude that the discrimination capacity of individual afferents of each type was inferior in humans than monkeys which could be because of differences in fingertip tissue compliance and skin friction.
AB - Dexterous object manipulation depends critically on information about forces normal and tangential to the fingerpads, and also on torque associated with object orientation at grip surfaces. We investigated how torque information is encoded by human tactile afferents in the fingerpads and compared them to 97 afferents recorded in monkeys (n=3; 2 females) in our previous study. Human data included slowly-adapting Type-II (SA-II) afferents, which are absent in the glabrous skin of monkeys. Torques of different magnitudes (3.5-7.5 mNm) were applied in clockwise and anticlockwise directions to a standard central site on the fingerpads of 34 human subjects (19 females). Torques were superimposed on a 2, 3, or 4 N background normal force. Unitary recordings were made from fast-adapting Type-I (FA-I, n=39), and slowly-adapting Type-I (SA-I, n=31) and Type-II (SA-II, n=13) afferents supplying the fingerpads via microelectrodes inserted into the median nerve. All three afferent types encoded torque magnitude and direction, with torque sensitivity being higher with smaller normal forces. SA-I afferent responses to static torque were inferior to dynamic stimuli in humans, while in monkeys the opposite was true. In humans this might be compensated by the addition of sustained SA-II afferent input, and their capacity to increase or decrease firing rates with direction of rotation. We conclude that the discrimination capacity of individual afferents of each type was inferior in humans than monkeys which could be because of differences in fingertip tissue compliance and skin friction.
KW - microneurography
KW - neural coding
KW - SA2
KW - tactile afferent
KW - torque
KW - touch
UR - http://www.scopus.com/inward/record.url?scp=85160966606&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.1305-22.2023
DO - 10.1523/JNEUROSCI.1305-22.2023
M3 - Article
C2 - 37142429
AN - SCOPUS:85160966606
SN - 0270-6474
VL - 43
SP - 4033
EP - 4046
JO - The Journal of Neuroscience
JF - The Journal of Neuroscience
IS - 22
ER -