Precise and stable edge orientation signaling by human first-order tactile neurons

  1. Vaishnavi Sukumar
  2. Roland S Johansson
  3. J Andrew Pruszynski  Is a corresponding author
  1. Western University, Canada
  2. Umeå University, Sweden

Abstract

Fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) first-order neurons in the human tactile system have distal axons that branch in the skin and form many transduction sites, yielding receptive fields with many highly sensitive zones or 'subfields'. We previously demonstrated that this arrangement allows FA-1 and SA-1 neurons to signal the geometric features of touched objects, specifically the orientation of raised edges scanned with the fingertips. Here we show that such signaling operates for fine edge orientation differences (5-20°) and is stable across a broad range of scanning speeds (15-180 mm/s); that is, under conditions relevant for real-world hand use. We found that both FA-1 and SA-1 neurons weakly signal fine edge orientation differences via the intensity of their spiking responses and only when considering a single scanning speed. Both neuron types showed much stronger edge orientation signaling in the sequential structure of the evoked spike trains and FA-1 neurons performed better than SA-1 neurons. Represented in the spatial domain, the sequential structure was strikingly invariant across scanning speeds, especially those naturally used in tactile spatial discrimination tasks. This speed invariance suggests that neurons' responses are structured via sequential stimulation of their subfields and thus links this capacity to their terminal organization in the skin. Indeed, the spatial precision of elicited action potentials rationally matched spatial acuity of subfield arrangements, which corresponds to a spatial period similar to the dimensions of individual fingertip ridges.

Data availability

Al the raw data generated as part of this study are publicly available.

The following data sets were generated

Article and author information

Author details

  1. Vaishnavi Sukumar

    Neuroscience Graduate Program, Western University, London, Canada
    Competing interests
    No competing interests declared.
  2. Roland S Johansson

    Department of Integrative Medical Biology, Umeå University, Umeå, Sweden
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3288-8326
  3. J Andrew Pruszynski

    Department of Physiology and Pharmacology, Western University, London, Canada
    For correspondence
    andrew.pruszynski@uwo.ca
    Competing interests
    J Andrew Pruszynski, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0786-0081

Funding

Vetenskapsrådet (22209)

  • J Andrew Pruszynski

Canadian Institutes of Health Research (Foundation Grant)

  • J Andrew Pruszynski

Canada Research Chairs (Tier 2)

  • J Andrew Pruszynski

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

Ethics

Human subjects: All participants provided written informed consent in accordance with the Declaration of Helsinki. The Umeå University ethics committee approved the study (PI: Johansson).

Reviewing Editor

  1. Hannes P Saal, University of Sheffield, United Kingdom

Publication history

  1. Preprint posted: June 3, 2022 (view preprint)
  2. Received: June 29, 2022
  3. Accepted: October 27, 2022
  4. Accepted Manuscript published: October 31, 2022 (version 1)
  5. Version of Record published: November 8, 2022 (version 2)

Copyright

© 2022, Sukumar et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Vaishnavi Sukumar
  2. Roland S Johansson
  3. J Andrew Pruszynski
(2022)
Precise and stable edge orientation signaling by human first-order tactile neurons
eLife 11:e81476.
https://doi.org/10.7554/eLife.81476

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