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

Vaishnavi Sukumar, Roland S. Johansson, View ORCID ProfileJ. Andrew Pruszynski
doi: https://doi.org/10.1101/2022.06.01.494420
Vaishnavi Sukumar
1Neuroscience Graduate Program, Western University, London, Canada
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Roland S. Johansson
2Department of Integrative Medical Biology, Umeå University, Umeå, Sweden
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J. Andrew Pruszynski
3Department of Physiology and Pharmacology, Western University, London, Canada
4Department of Psychology, Western University, London, Canada
5Western Institute of Neuroscience, Western University, London, Canada
6Robarts Research Institute, Western University, London, Canada
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  • ORCID record for J. Andrew Pruszynski
  • For correspondence: andrew.pruszynski@uwo.ca
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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. Indeed, the spatial precision of elicited action potentials rationally matched spatial acuity of subfield arrangements, which typically corresponds to the dimension of individual fingertip ridges. The present results further the idea that the terminal branching of first-order tactile neurons constitutes a peripheral neural mechanism supporting the identification of tactile geometric features.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 03, 2022.
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Precise and stable edge orientation signaling by human first-order tactile neurons
Vaishnavi Sukumar, Roland S. Johansson, J. Andrew Pruszynski
bioRxiv 2022.06.01.494420; doi: https://doi.org/10.1101/2022.06.01.494420
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Precise and stable edge orientation signaling by human first-order tactile neurons
Vaishnavi Sukumar, Roland S. Johansson, J. Andrew Pruszynski
bioRxiv 2022.06.01.494420; doi: https://doi.org/10.1101/2022.06.01.494420

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