Cited by 421Tactile and Sensory InteractionsMotor Control and AdaptationVisual perception and processing mechanisms

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Spatial and temporal codes mediate the tactile perception of natural textures

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Weber, Alison I., Saal, Hannes P., Lieber, Justin D., Cheng, Ju-Wen, Manfredi, Louise R., Dammann, John F., Bensmaia, Sliman J.·2013·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1305509110PMC PMC3800989

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Abstract

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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Background
A spatial code for temporal cues is necessary for sensory learningPreprint
Bagur, S., Bourg, J., Kempf, A., Tarpin, T., Bergaoui, K., Guo, Y., Ceballo, S., Schwenkgrub, J., Verdier, A., Puel, J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.14.520391 · Cited by 5
Decoding roughness perception in distributed haptic devices
Chatterjee, S., Tan, S., Choi, C., Kuchibhotla, A., Wan, G., Peshkin, M. A., Colgate, J. E., & Hipwell, M. C. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae468 · Cited by 4
“It has been observed that all three afferent classes contribute to roughness perception (9, 10) and that for most natural textures, the variation in RA-1 activation is a more accurate predictor of roughness than SA-1 activation (10).”
BackgroundMethodInfluential
Vibroacoustic signatures: proof of concept for simple material characterization during needle interventions
Steeg, K., Serwatka, W., Rzepka, D., Oran, H., Özdil, O. B., Heryan, K., Krombach, G. A., & Friebe, M. (2025) · International Journal of Computer Assisted Radiology and Surgery · doi:10.1007/s11548-025-03492-0 · Cited by 4
Simultaneous encoding of sensory features: the role of multiplexing and noise in tactile perception and neural representation
Kamaleddin, M. A. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70093 · Cited by 4
Cortical stimulation for somatosensory feedback: translation from nonhuman primates to clinical applications
Badi, M., Borgognon, S., O’Doherty, J. E., & Shokur, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822828-9.00008-3 · Cited by 4
Humans Use a Temporally Local Code for Vibrotactile Perception
Bhattacharjee, A., Braun, C., & Schwarz, C. (2021) · eNeuro · doi:10.1523/eneuro.0263-21.2021 · Cited by 4
“The predominant engagement of model PCs and qualitative fit with psychometrics does not come as a surprise as it is a common finding that PCs are the most sensitive afferents to indenting vibrotactile stimuli (Johansson, 1978) as well as to touch of more natural surfaces (Weber et al., 2013).”
Background
Neuromorphic Tactile Sensing and Encoding
Kumar, D., Silva, A. N., & Thakor, N. V. (2023) · Handbook of Neuroengineering · doi:10.1007/978-981-16-5540-1_117 · Cited by 4
When mechanical engineering inspired from physiology improves postural-related somatosensory processes
Sutter, C., Fabre, M., Massi, F., Blouin, J., & Mouchnino, L. (2023) · Scientific Reports · doi:10.1038/s41598-023-45381-z · Cited by 4
“Similarly, the interaction of the foot and the biomimetic surface increases the intensity of the skin mechanoreceptors stimulation, which in turn boosted the transmission of cutaneous signals to the primary somatosensory cortex (SI) where neurons respond to various tactile stimulations (e.g., Bensmaia et al. 2008; Web…”
Background
The suppression of lower leg electromyography when walking in textured foot orthoses
Robb, K. A., & Perry, S. D. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06904-w · Cited by 4
“…surfaces is maximized when skin is stretched and indented to sufficiently generate an influx of temporal spiking patterns from cutaneous affer-ents (Weber et al. 2013) and the altered tactile feedback is relayed to the spinal cord (afferent volley of the cutaneous reflex loop) (Robb et al. 2022).”
General Sensory System and Taste
Palmieri, M., Caldas, G. D. C., Monroy-Sosa, A., Lopez, I. G., Rea, N. S., Cortés-Contreras, A. P., & Ascenzi, B. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822404-5.00004-8 · Cited by 4
Cortical Representation of Tactile Stickiness Evoked by Skin Contact and Glove Contact
Kim, J., Bülthoff, I., & Bülthoff, H. (2020) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2020.00019 · Cited by 4
Coupling of single cutaneous afferents in the hand with ankle muscles, and their response to rapid light touch displacements
Toth, A. L., Fenrich, K. K., Jones, K. E., & Misiaszek, J. E. (2022) · Journal of Neurophysiology · doi:10.1152/jn.00280.2021 · Cited by 4
Multiple Spatial Spectral Components of Static Skin Deformation for Predicting Macroscopic Roughness Perception
Sun, Q., Okamoto, S., Akiyama, Y., & Yamada, Y. (2022) · IEEE Transactions on Haptics · doi:10.1109/toh.2022.3199082 · Cited by 4
“These studies [18], [25], [26], [27] considered the existence of an optimal wavelength for the Gabor”
BackgroundMethodResultInfluential
Probing the Neurophysiology of Temporal Sensitivity in the Somatosensory System Using the Mismatch Negativity (MMN) Sensory Memory Paradigm
Isenstein, E. L., Freedman, E. G., Xu, J., DeAndrea-Lazarus, I. A., & Foxe, J. J. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.013 · Cited by 5
More than the Sum of its Parts: Perception and Neuronal Underpinnings of Sequence Processing
Maravall, M., Ostojic, S., Pressnitzer, D., & Maria Chait, A. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.07.043 · Cited by 4
“In touch, contact with an object elicits a sequence of skin vibrations whose temporal structure provides information about object texture and motion (Weber et al., 2013).”
Background
Neuroprosthetics
Ziat, M., & Bensmaı̈a, S. J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-08-097086-8.55057-0 · Cited by 4
Exploring Fingertip Slip Feedback for Haptic Augmentation and Referral Using Thermal Feedback
Kim, D., Lim, C., & Park, G. (2025) · IEEE World Haptics Conference (WHC) · doi:10.1109/whc64065.2025.11123352 · Cited by 3
“Both methods effectively rendered the fine textures’ roughness by stimulating the Pacinian corpuscle (PC) [8] or activating both PC and rapidly adapting (RA) fibers [9].”
Understanding the inference and design of haptic experiences
Dalsgaard, T.-S., Bergström, J., & Hornbæk, K. (2025) · International Journal of Human-Computer Studies · doi:10.1016/j.ijhcs.2025.103598 · Cited by 4
Recent Advances in Neuromorphic Tactile Perception for Robotic Applications
Zhang, Z., & Lee, C. (2026) · AI Sensors · doi:10.3390/aisens2010003 · Cited by 3
“These receptors translate mechanical deformation into neural spike patterns [7,8].”
Cascade Amplification Effect for Mechanical Stimuli Sensors by Designing the Current Path Through Carbon Fiber Beams
Hu, J., Chen, Z., Lao, K., Liang, H., Huang, X., Li, Z., Huang, J., Hu, X., Liang, B., Ye, D., et al. (2021) · IEEE Sensors Journal · doi:10.1109/jsen.2021.3083674 · Cited by 3
Differential Recovery of Submodality Touch Neurons and Interareal Communication in Sensory Input-Deprived Area 3b and S2 Cortices
Wu, R., Yang, P., Wang, F., Liu, Q., Gore, J. C., & Chen, L. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0034-22.2022 · Cited by 3
Cutaneous and Muscle Mechanoreceptors: Sensitivity to Mechanical Vibrations
Ribot‐Ciscar, E. (2020) · Springer eBooks · doi:10.1007/978-3-030-43985-9_6 · Cited by 3
Raised Dot Enumeration Via Haptic Exploration
Sharma, P. K., Britto, A. P., Aggarwal, N., & Hughes, B. G. (2020) · IEEE Transactions on Haptics · doi:10.1109/toh.2020.3018727 · Cited by 3
“…of mechanoreceptors that respond preferentially to either large or low amplitude skin deformation, and high-or low-frequency changes in stimulation [22], [23], and it gives rise to both precise discrimination of differences in texture [24] as well as perceptual constancies across wide variation in…”
Background
Effects of receptor density on the tactile perception of roughness: implications for neural mechanisms of texture perception
Gescheider, G. A., & Wright, J. H. (2021) · Somatosensory & Motor Research · doi:10.1080/08990220.2021.1949976 · Cited by 2
Objective neuromodulation basis for intrafascicular artificial somatosensation through carbon nanotube yarn electrodes
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Global surface features contribute to human haptic roughness estimations
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Artificial Sensory Feedback to the Brain: Somatosensory Feedback for Neural Devices and BCI
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Temporally Local Tactile Codes Can Be Stored in Working Memory
Bhattacharjee, A., & Schwarz, C. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.840108 · Cited by 3
The Tactile Distance Aftereffect Transfers to Roughness Perception
Jeschke, M., Drewing, K., & Azañón, E. (2023) · IEEE World Haptics Conference (WHC) · doi:10.1109/whc56415.2023.10224476 · Cited by 3

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)
ORCID: Weber, Alison I.
Saal, Hannes P.
Lieber, Justin D.
Manfredi, Louise R.
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
DOI: 10.1073/pnas.1305509110
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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Spatial and temporal codes mediate the tactile perception of natural textures

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