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Pre-neuronal morphological processing of object location by individual whiskers

Nature Neuroscience volume 16, pages 622–631 (2013)Cite this article

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Abstract

In the vibrissal system, touch information is conveyed by a receptorless whisker hair to follicle mechanoreceptors, which then provide input to the brain. We examined whether any processing, that is, meaningful transformation, occurs in the whisker itself. Using high-speed videography and tracking the movements of whiskers in anesthetized and behaving rats, we found that whisker-related morphological phase planes, based on angular and curvature variables, can represent the coordinates of object position after contact in a reliable manner, consistent with theoretical predictions. By tracking exposed follicles, we found that the follicle-whisker junction is rigid, which enables direct readout of whisker morphological coding by mechanoreceptors. Finally, we found that our behaving rats pushed their whiskers against objects during localization in a way that induced meaningful morphological coding and, in parallel, improved their localization performance, which suggests a role for pre-neuronal morphological computation in active vibrissal touch.

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Figure 1: Effects of object position on morphological and kinematic variables in artificially whisking anesthetized rats.
Figure 2: Mechanical encoding of object location by whiskers of artificially whisking anesthetized rats.
Figure 3: Morphological encoding in the Gκ-θa phase plane.
Figure 4: Angle and global curvature dynamics in freely moving rats during a localization task.
Figure 5: Curvature at the whisker base and along the whisker shaft in anesthetized rats.
Figure 6: Angle and base curvature dynamics in awake, head-fixed rats.
Figure 7: Single-cycle, single-whisker morphological encoding in the Bκ-θp phase plane.
Figure 8: Follicle mechanics during active vibrissal touch.

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Acknowledgements

We thank D. Goldian and S. Haidarliu for technical assistance, N. Rubin for programming, B. Schick for reviewing, M. Hartmann and J. Solomon for critically reading the manuscript and for extensive and helpful discussions, and C. Moore, J. Ritt, L. Gomez, S. Barash and G. Bi for helpful suggestions. The article is dedicated to our late friend and colleague Maciej Pietr for his significant contribution to this work. This work was supported by the Israel Science Foundation (grant 749/10), the Minerva Foundation funded by the Federal German Ministry for Education and Research, the United States–Israel Binational Science Foundation (grant 2011432), the Ministry of Science and Technology (Israel), the Ministry of Research (Taiwan), and the Chief Scientist, Israeli Ministry of Health. K.B. acknowledges support by the KAMEA program administered by the Ministry of Absorption (Israel). P.M.K. was supported by a Long-Term Fellowship from the Human Frontier Science Program. E.A. holds the Helen Diller Family Professorial Chair of Neurobiology.

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Author notes

  1. Maciej Pietr: Deceased.

  2. Knarik Bagdasarian, Marcin Szwed, Per Magne Knutsen and Dudi Deutsch: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel

    Knarik Bagdasarian, Dudi Deutsch, Maciej Pietr & Ehud Ahissar

  2. Psychophysiology Laboratory, Institute of Psychology, Jagiellonian University, Kraków, Poland

    Marcin Szwed

  3. Department of Physics, University of California, San Diego, La Jolla, California, USA

    Per Magne Knutsen

  4. Rappaport Faculty of Medicine, Technion, Haifa, Israel

    Dori Derdikman

  5. Department of Psychology and the Neuroscience Institute, Princeton University, Princeton, New Jersey, USA

    Erez Simony

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Contributions

K.B. and M.S. performed the artificial whisking experiments. K.B. designed and K.B. and M.S. performed the exposed follicle experiments. P.M.K., D. Deutsch and M.P. performed the head-fixed and freely moving experiments. K.B., M.S., P.M.K., D. Deutsch, D. Derdikman and E.S. analyzed data. K.B., M.S., P.M.K., D. Deutsch, D. Derdikman, E.S. and E.A. prepared figures. K.B., M.S., P.M.K., D. Deutsch, D. Derdikman and E.A. wrote the manuscript.

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Correspondence to Ehud Ahissar.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figure 1 (PDF 16 kb)

Supplementary Movie 1

Freely-moving rat (single whisker) (AVI 4463 kb)

Supplementary Movie 2

Freely-moving rat (intact pad) (AVI 2747 kb)

Supplementary Movie 3

Head-fixed rat (AVI 869 kb)

Supplementary Movie 4

Follicle-whisker dynamics (MOV 9554 kb)

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Bagdasarian, K., Szwed, M., Knutsen, P. et al. Pre-neuronal morphological processing of object location by individual whiskers. Nat Neurosci 16, 622–631 (2013). https://doi.org/10.1038/nn.3378

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