Edge-orientation processing in first-order tactile neurons
Abstract
A fundamental feature of first-order neurons in the tactile system is that their distal axon branches in the skin and forms many transduction sites, yielding complex receptive fields with many highly sensitive zones. We found that this arrangement constitutes a peripheral neural mechanism that allows individual neurons to signal geometric features of touched objects. Specifically, we observed that two types of first-order tactile neurons that densely innervate the glabrous skin of the human fingertips signaled edge orientation via both the intensity and the temporal structure of their responses. Moreover, we found that the spatial layout of a neuron's highly sensitive zones predicted its sensitivity to particular edge orientations. We submit that peripheral neurons in the touch-processing pathway, as with peripheral neurons in the visual-processing pathway, perform feature extraction computations that are typically attributed to neurons in the cerebral cortex.
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Certain key features of the object, such as the presence and orientation of edges, are enhanced at the periphery due to skin mechanics and the geometry of the receptive fields.
“Certain key features of the object, for example the presence and orientation of edges, are enhanced at the periphery due to skin mechanics (Fig. 4A) (Phillips and Johnson, 1981;Sripati et al., 2006) and the geometry of the receptive fields (Pruszynski and Johansson, 2014).”
From Biomimetic approaches to bionic touch through a peripheral nerve interface (2015) · cites this paper as Pruszynski and Johansson, 2014
Receptive fields of type I afferents are not uniform but contain several individual subfields or hot spots in both glabrous and hairy skin.
“The reasoning above ignores the fact that receptive fields of type I afferents are not uniform but contain several individual subfields or hot spots, as demonstrated in both glabrous (Johansson 1978;Pruszynski and Johansson 2014) and hairy skin (Vallbo et al. 1995).”
From Tactile innervation densities across the whole body (2020) · cites this paper as Pruszynski and Johansson 2014
Cites
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Johansson, R. S., & Flanagan, J. R. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2621 · Cited by 2,063 · see citing works
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Self-citationThe single dendritic branch as a fundamental functional unit in the nervous system
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The representation of stimulus orientation in the early stages of somatosensory processing
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Analogous intermediate shape coding in vision and touch
Yau, J. M., Pasupathy, A., Fitzgerald, P. J., Hsiao, S. S., & Connor, C. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904186106 · Cited by 77 · see citing works
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A bioinspired flexible organic artificial afferent nerve
Kim, Y., Chortos, A., Xu, W., Liu, Y., Oh, J. Y., Son, D., Kang, J., Foudeh, A. M., Zhu, C., Lee, Y., et al. (2018) · Science · doi:10.1126/science.aao0098 · Cited by 1,466 · see citing works
Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain
Osborn, L. E., Dragomir, A., Betthauser, J. L., Hunt, C. L., Nguyen, H. H., Kaliki, R. R., & Thakor, N. V. (2018) · Science Robotics · doi:10.1126/scirobotics.aat3818 · Cited by 427 · see citing works
Tactile innervation densities across the whole body
Corniani, G., & Saal, H. P. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00313.2020 · Cited by 396 · see citing works
Neural Basis of Touch and Proprioception in Primate Cortex
Delhaye, B. P., Long, K. H., & Bensmaia, S. J. (2018) · Comprehensive Physiology · doi:10.1002/cphy.c170033 · Cited by 214 · see citing works
Biomimetic approaches to bionic touch through a peripheral nerve interface
Saal, H. P., & Bensmaia, S. J. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.06.010 · Cited by 179 · see citing works
“, 2006) and the geometry of the receptive fields (Pruszynski and Johansson, 2014).”
- Authors
- Pruszynski, J. A., & Johansson, R. S.
- Affiliations
- Umeå University (SE)
- Corresponding author
- Pruszynski, J Andrew
- Venue
- Nature Neuroscience
- Published
- 2014-08-31
- Volume
- 17
- Issue
- 10
- Pages
- 1404-1409
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2091789155
- Cited by
- 207
- References
- 5
- Citations by year
- 2026: 13 · 2025: 12 · 2024: 29 · 2023: 4 · 2022: 25 · 2021: 23 · 2020: 19 · 2019: 16 · 2018: 18 · 2017: 14 · 2016: 18 · 2015: 14 · 2014: 2
- FWCI
- 8.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Karolinska Institutet
- Vetenskapsrådet
- University of Tennessee Space Institute
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- edge orientation, receptive fields, dendritic branching, glabrous skin, feature extraction, temporal coding, intensity coding, object shape perception
- MeSH terms
- Action Potentials, Adult, Afferent Pathways, Brain Mapping, Female, Humans, Male, Models, Neurological, Motion Perception, Neurons, Orientation, Predictive Value of Tests, ROC Curve, Somatosensory Cortex, Time Factors, Touch, Young Adult
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