The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Spatial and temporal codes mediate the tactile perception of natural textures
Open accessAbstract
When we run our fingers over the surface of an object, we acquire information about its microgeometry and material properties. Texture information is widely believed to be conveyed in spatial patterns of activation evoked across one of three populations of cutaneous mechanoreceptive afferents that innervate the fingertips. Here, we record the responses evoked in individual cutaneous afferents in Rhesus macaques as we scan a diverse set of natural textures across their fingertips using a custom-made rotating drum stimulator. We show that a spatial mechanism can only account for the processing of coarse textures. Information about most natural textures, however, is conveyed through precise temporal spiking patterns in afferent responses, driven by high-frequency skin vibrations elicited during scanning. Furthermore, these texture-specific spiking patterns predictably dilate or contract in time with changes in scanning speed; the systematic effect of speed on neuronal activity suggests that it can be reversed to achieve perceptual constancy across speeds. The proposed temporal coding mechanism involves converting the fine spatial structure of the surface into a temporal spiking pattern, shaped in part by the mechanical properties of the skin, and ascribes an additional function to vibration-sensitive mechanoreceptive afferents. This temporal mechanism complements the spatial one and greatly extends the range of tangible textures. We show that a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture.
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“These skin oscillations in turn evoke highly patterned and repeatable temporal spiking patterns in PC and to some extent RA fibers, and these millisecond precision spiking patterns convey information about textural features too fine to be encoded spatially (Weber et al., 2013).”
From Biomimetic approaches to bionic touch through a peripheral nerve interface (2015) · cites this paper as Weber et al., 2013
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BackgroundMethodResultInfluentialEffect of scanning speed on texture-elicited vibrations
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“Implications for tactile texture perception Texture perception is highly independent of scanning speed and contact force despite the fact that the response of the skin and that of tactile nerve fibres is highly dependent on these exploratory parameters [6,22].”
BackgroundTexture recognition based on multi-sensory integration of proprioceptive and tactile signals
Rostamian, B., Koolani, M., Abdollahzade, P., Lankarany, M., Falotico, E., Amiri, M., & Thakor, N. V. (2022) · Scientific Reports · doi:10.1038/s41598-022-24640-5 · Cited by 40
Feeling fooled: Texture contaminates the neural code for tactile speed
Delhaye, B. P., O'Donnell, M. K., Lieber, J. D., McLellan, K. R., & Bensmaı̈a, S. J. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000431 · Cited by 42
Tactile Acuity Charts: A Reliable Measure of Spatial Acuity
Bruns, P., Camargo, C. J., Campanella, H., Estéve, J., Dinse, H. R., & Röder, B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087384 · Cited by 39
“Such a temporal code seems to underlie the representation of fine textures in the peripheral nerve, but might, however, not be sufficient for dissolving their spatial layout [71] as required in the tactile acuity charts.”
BackgroundRyun, S., Kim, J. S., Lee, H., & Chung, C. K. (2017) · Scientific Reports · doi:10.1038/s41598-017-15767-x · Cited by 39
The role of vibration in tactile speed perception
Dallmann, C. J., Ernst, M. O., & Moscatelli, A. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00621.2015 · Cited by 38
Data-Driven Texture Rendering on an Electrostatic Tactile Display
Ilkhani, G., Aziziaghdam, M., & Samur, E. (2017) · International Journal of Human-Computer Interaction · doi:10.1080/10447318.2017.1286766 · Cited by 38
“, 2007; Yoshioka, Gibb, Dorsch, Hsiao, & Johnson, 2001) and finer features are encoded temporally (Weber et al., 2013).”
MethodBrain networks underlying tactile softness perception: A functional magnetic resonance imaging study
Kitada, R., Doizaki, R., Kwon, J., Tanigawa, T., Nakagawa, E., Kochiyama, T., Kajimoto, H., Sakamoto, M., & Sadato, N. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.04.044 · Cited by 38
Mazzoni, A., Oddo, C. M., Valle, G., Camboni, D., Strauss, I., Barbaro, M., Barabino, G., Puddu, R., Carboni, C., Bisoni, L., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-57454-4 · Cited by 40
Sensory computations in the cuneate nucleus of macaques
Suresh, A. K., Greenspon, C. M., He, Q., Rosenow, J. M., Miller, L. E., & Bensmaı̈a, S. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2115772118 · Cited by 36
“While each submodality might be more responsive to any one stimulus feature, information about most features is distributed over all three submodalities, and the resulting perceptual experience reflects this integration (7, 21, 28, 29).”
BackgroundMethodInfluentialThe language of the brain: real-world neural population codes
Pruszynski, J. A., & Zylberberg, J. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.06.005 · Cited by 33
Engineered Mechanosensors Inspired by Biological Mechanosensilla
Wang, Q., Fan, C., Gui, Y., Zhang, L., Zhang, J., Sun, L., Wang, K., & Han, Z. (2021) · Advanced Materials Technologies · doi:10.1002/admt.202100352 · Cited by 36
Perceptual Spaces: Mathematical Structures to Neural Mechanisms
Zaidi, Q., Victor, J. D., McDermott, J. H., Geffen, M. N., Bensmaı̈a, S. J., & Cleland, T. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3343-13.2013 · Cited by 40
“Judgments of roughness, the dominant dimension of texture, are well predicted based on a combination of spatial and temporal codes (Weber et al., 2013), suggesting that temporal representations of fine spatial features are combined with spatial representations of coarse features to culminate in a holistic percept of s…”
BackgroundRekik, Y., Vezzoli, E., Grisoni, L., & Giraud, F. (2017) · CHI Conference on Human Factors in Computing Systems · doi:10.1145/3025453.3026010 · Cited by 36
“Just like real texture ( e.g. , plastic, glass, etc), a tactile texture refers to a sequence of periodic tactile feedback [21, 20] such that the period to be reproduced inside the texture can be formed by some specific signal (periodic, structured noise, micro-geometry extracted, etc...).”
BackgroundFeeling fine - the effect of topography and friction on perceived roughness and slipperiness
Arvidsson, M., Ringstad, L., Skedung, L., Duvefelt, K., & Rutland, M. W. (2017) · Biotribology · doi:10.1016/j.biotri.2017.01.002 · Cited by 35
Genna, C., Oddo, C. M., Fanciullacci, C., Chisari, C., Jörntell, H., Artoni, F., & Micera, S. (2017) · Brain Topography · doi:10.1007/s10548-017-0569-8 · Cited by 35
Fins as Mechanosensors for Movement and Touch-Related Behaviors
Aiello, B. R., Hardy, A. R., Westneat, M. W., & Hale, M. E. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy065 · Cited by 34
Eck, J., Kaas, A. L., Mulders, J. L. J., Hausfeld, L. G., Kourtzi, Z., & Goebel, R. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu294 · Cited by 34
The neural basis of tactile texture perception
Lieber, J. D., & Bensmaı̈a, S. J. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102621 · Cited by 36
A Digital Hardware Realization for Spiking Model of Cutaneous Mechanoreceptor
Salimi-Nezhad, N., Amiri, M., Falotico, E., & Laschi, C. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00322 · Cited by 33
“…link between the first and the second order neurons (mechanoreceptors and cuneate cells, respectively) has not been completely explored, and computational and experimental findings on how information is processed along this pathway are still required (Weber et al., 2013; Saal and Bensmaia, 2014).”
BackgroundResultBio-Inspired Haptic Feedback for Artificial Palpation in Robotic Surgery
Ouyang, Q., Wu, J., Sun, S., Pensa, J. W., Abiri, A., Dutson, E., & Bisley, J. W. (2021) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2021.3076094 · Cited by 35
Texture is encoded in precise temporal spiking patterns in primate somatosensory cortex
Long, K. H., Lieber, J. D., & Bensmaı̈a, S. J. (2022) · Nature Communications · doi:10.1038/s41467-022-28873-w · Cited by 31
Mechanical Vibration Influences the Perception of Electrovibration
Ryu, S., Pyo, D., Lim, S.-C., & Kwon, D.-S. (2018) · Scientific Reports · doi:10.1038/s41598-018-22865-x · Cited by 31
Ultrafast readout, crosstalk suppression iontronic array enabled by frequency-coding architecture
Li, Z., Yang, J., Zhang, Y., Geng, P., Feng, J., Chen, B., Zhang, X., Yuan, G., Chen, X., & Wang, T. (2024) · npj Flexible Electronics · doi:10.1038/s41528-024-00295-2 · Cited by 33
Bioinspired Adaptive Sensors: A Review on Current Developments in Theory and Application
Gong, G., Zhou, Y., Li, Q., Zhao, W., Geng, S., Li, H., Leng, Y., Zhu, S., Ding, G., Zhai, Y., et al. (2025) · Advanced Materials · doi:10.1002/adma.202505420 · Cited by 31
Metadata
- Authors
- Weber, A. I., Saal, H. P., Lieber, J. D., Cheng, J.-W., Manfredi, L. R., Dammann, J. F., & Bensmaia, S. J.
- Affiliations
- Department of Organismal Biology and Anatomy and
- University of Chicago (US)
- Chang Gung Memorial Hospital (TW)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-09-30
- Volume
- 110
- Issue
- 42
- Pages
- 17107-17112
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3800989
- OpenAlex
- W2147698153
- Cited by
- 421
- References
- 39
- Citations by year
- 2026: 37 · 2025: 37 · 2024: 37 · 2023: 27 · 2022: 58 · 2021: 47 · 2020: 38 · 2019: 34 · 2018: 28 · 2017: 23 · 2016: 23 · 2015: 17 · 2014: 13 · 2013: 2
- FWCI
- 10.02
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- other-oa
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- tactile texture perception, cutaneous mechanoreceptors, temporal coding, spatial coding, skin vibration, scanning speed, perceptual constancy, natural textures, rhesus monkeys, skin biomechanics
- MeSH terms
- Adolescent, Adult, Animals, Female, Fingers, Humans, Macaca mulatta, Male, Synaptic Transmission, Skin, Surface Properties, Vibration, Touch Perception
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