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Pre-neuronal morphological processing of object location by individual whiskers

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 -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 -θp phase plane.
Figure 8: Follicle mechanics during active vibrissal touch.

References

  1. Kleinfeld, D., Ahissar, E. & Diamond, M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Diamond, M.E., von Heimendahl, M., Knutsen, P.M., Kleinfeld, D. & Ahissar, E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601–612 (2008).

    Article  CAS  PubMed  Google Scholar 

  3. Ebara, S., Kumamoto, K., Matsuura, T., Mazurkiewicz, J.E. & Rice, F.L. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. J. Comp. Neurol. 449, 103–119 (2002).

    Article  PubMed  Google Scholar 

  4. Hartmann, M.J., Johnson, N.J., Towal, R.B. & Assad, C. Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal. J. Neurosci. 23, 6510–6519 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ritt, J.T., Andermann, M.L. & Moore, C.I. Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats. Neuron 57, 599–613 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wolfe, J. et al. Texture coding in the rat whisker system: slip-stick versus differential resonance. PLoS Biol. 6, e215 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Szwed, M., Bagdasarian, K. & Ahissar, E. Encoding of vibrissal active touch. Neuron 40, 621–630 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Szwed, M. et al. Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J. Neurophysiol. 95, 791–802 (2006).

    Article  PubMed  Google Scholar 

  9. Lottem, E. & Azouz, R. Dynamic translation of surface coarseness into whisker vibrations. J. Neurophysiol. 100, 2852–2865 (2008).

    Article  PubMed  Google Scholar 

  10. Arabzadeh, E., Zorzin, E. & Diamond, M.E. Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol. 3, e17 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Andermann, M.L., Ritt, J., Neimark, M.A. & Moore, C.I. Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli. Neuron 42, 451–463 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. Knutsen, P.M. & Ahissar, E. Orthogonal coding of object location. Trends Neurosci. 32, 101–109 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Kleinfeld, D. & Deschênes, M. Neuronal basis for object location in the vibrissa scanning sensorimotor system. Neuron 72, 455–468 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Birdwell, J.A. et al. Biomechanical models for radial distance detection by rat vibrissae. J. Neurophysiol. 98, 2439–2455 (2007).

    Article  PubMed  Google Scholar 

  15. Quist, B.W. & Hartmann, M.J. Mechanical signals at the base of a rat vibrissa: the effect of intrinsic vibrissa curvature and implications for tactile exploration. J. Neurophysiol. 107, 2298–2312 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Solomon, J.H. & Hartmann, M.J. Radial distance determination in the rat vibrissal system and the effects of Weber's law. Phil. Trans. R. Soc. Lond. B 366, 3049–3057 (2011).

    Article  Google Scholar 

  17. Boubenec, Y., Shulz, D.E. & Debregeas, G. Whisker encoding of mechanical events during active tactile exploration. Front. Behav. Neurosci. 6, 74 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Knutsen, P.M., Derdikman, D. & Ahissar, E. Tracking whisker and head movements in unrestrained behaving rodents. J. Neurophysiol. 93, 2294–2301 (2005).

    Article  PubMed  Google Scholar 

  19. Pearson, M.J., Mitchinson, B., Sullivan, J.C., Pipe, A.G. & Prescott, T.J. Biomimetic vibrissal sensing for robots. Phil. Trans. R. Soc. Lond. B 366, 3085–3096 (2011).

    Article  Google Scholar 

  20. Prescott, T.J., Pearson, M.J., Mitchinson, B., Sullivan, J.C.W. & Pipe, A.G. Whisking with robots. IEEE Robot. Autom. Mag. 16, 42–50 (2009).

    Article  Google Scholar 

  21. Towal, R.B., Quist, B.W., Gopal, V., Solomon, J.H. & Hartmann, M.J. The morphology of the rat vibrissal array: a model for quantifying spatiotemporal patterns of whisker-object contact. PLoS Comput. Biol. 7, e1001120 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pfeifer, R. & Gomez, G. Morphological computation: connecting brain, body and environment. in Creating Brain-like Intelligence: From Basic Principles to Complex Intelligent Systems (eds. Sendhoff, B., Körner, E., Sporns, O., Ritter, H. & Doya, K.) 66–83 (2009).

  23. Knutsen, P.M., Pietr, M. & Ahissar, E. Haptic object localization in the vibrissal system: behavior and performance. J. Neurosci. 26, 8451–8464 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. O'Connor, D.H. et al. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 30, 1947–1967 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Deutsch, D., Pietr, M., Knutsen, P.M., Ahissar, E. & Schneidman, E. Fast feedback in active sensing: touch-induced changes to whisker-object interaction. PLoS ONE 7, e44272 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Mitchinson, B., Martin, C.J., Grant, R.A. & Prescott, T.J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 274, 1035–1041 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  27. O'Regan, J.K. & Noe, A. A sensorimotor account of vision and visual consciousness. Behav. Brain Sci. 24, 939–973, discussion 973–1031 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. Euler, L. Eneström Number 65: Methodus Inveniendi Lineas Curvas Maximi Minimive Proprietate Gaudentes, Sive Solutio Problematis Isoperimetrici Lattissimo Sensu Accepti (Marcum-Michaelem Bousquet and Socios, Geneva, 1744).

  29. Hill, D.N., Curtis, J.C., Moore, J.D. & Kleinfeld, D. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 72, 344–356 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gordon, G. & Ahissar, E. Hierarchical curiosity loops and active sensing. Neural Netw. 32, 119–129 (2012).

    Article  PubMed  Google Scholar 

  31. Ahissar, E., Abeles, M., Ahissar, M., Haidarliu, S. & Vaadia, E. Hebbian-like functional plasticity in the auditory cortex of the behaving monkey. Neuropharmacology 37, 633–655 (1998).

    Article  CAS  PubMed  Google Scholar 

  32. Ego-Stengel, V., Shulz, D.E., Haidarliu, S., Sosnik, R. & Ahissar, E. Acetylcholine-dependent induction and expression of functional plasticity in the barrel cortex of the adult rat. J. Neurophysiol. 86, 422–437 (2001).

    Article  CAS  PubMed  Google Scholar 

  33. Bahar, A., Dudai, Y. & Ahissar, E. Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat. J. Neurophysiol. 92, 3298–3308 (2004).

    Article  PubMed  Google Scholar 

  34. Saig, A., Gordon, G., Assa, E., Arieli, A. & Ahissar, E. Motor-sensory confluence in tactile perception. J. Neurosci. 32, 14022–14032 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ahissar, E. & Knutsen, P.M. Object localization with whiskers. Biol. Cybern. 98, 449–458 (2008).

    Article  PubMed  Google Scholar 

  36. Horev, G. et al. Motor-sensory convergence in object localization: a comparative study in rats and humans. Phil. Trans. R. Soc. Lond. B 366, 3070–3076 (2011).

    Article  Google Scholar 

  37. Mitchinson, B. et al. Empirically inspired simulated electro-mechanical model of the rat mystacial follicle-sinus complex. Proc. Biol. Sci. 271, 2509–2516 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lottem, E. & Azouz, R. A unifying framework underlying mechanotransduction in the somatosensory system. J. Neurosci. 31, 8520–8532 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hill, D.N., Bermejo, R., Zeigler, H.P. & Kleinfeld, D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity. J. Neurosci. 28, 3438–3455 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Simony, E. et al. Temporal and spatial characteristics of vibrissa responses to motor commands. J. Neurosci. 30, 8935–8952 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Haidarliu, S., Simony, E., Golomb, D. & Ahissar, E. Muscle architecture in the mystacial pad of the rat. Anat. Rec. (Hoboken) 293, 1192–1206 (2010).

    Article  Google Scholar 

  42. Stüttgen, M.C., Kullmann, S. & Schwarz, C. Responses of rat trigeminal ganglion neurons to longitudinal whisker stimulation. J. Neurophysiol. 100, 1879–1884 (2008).

    Article  PubMed  Google Scholar 

  43. Pammer, L. et al. The mechanical variables underlying object localization along the axis of the whisker. J. Neurosci. (in the press) (2013).

  44. O'Connor, D.H., Peron, S.P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048–1061 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Knutsen, P.M., Biess, A. & Ahissar, E. Vibrissal kinematics in 3D: tight coupling of azimuth, elevation, and torsion across different whisking modes. Neuron 59, 35–42 (2008).

    Article  CAS  PubMed  Google Scholar 

  46. Sachdev, R.N., Sato, T. & Ebner, F.F. Divergent movement of adjacent whiskers. J. Neurophysiol. 87, 1440–1448 (2002).

    Article  PubMed  Google Scholar 

  47. Chiel, H.J., Ting, L.H., Ekeberg, Ö. & Hartmann, M.J.Z. The brain in its body: motor control and sensing in a biomechanical context. J. Neurosci. 29, 12807–12814 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cramer, N.P. & Keller, A. Cortical control of a whisking central pattern generator. J. Neurophysiol. 96, 209–217 (2006).

    Article  PubMed  Google Scholar 

  49. Harish, O. & Golomb, D. Control of the firing patterns of vibrissa motoneurons by modulatory and phasic synaptic inputs: a modeling study. J. Neurophysiol. 103, 2684–2699 (2010).

    Article  PubMed  Google Scholar 

  50. Herfst, L.J. & Brecht, M. Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. J. Neurophysiol. 99, 2821–2832 (2008).

    Article  PubMed  Google Scholar 

  51. Pietr, M.D., Knutsen, P.M., Shore, D.I., Ahissar, E. & Vogel, Z. Cannabinoids reveal separate controls for whisking amplitude and timing in rats. J. Neurophysiol. 104, 2532–2542 (2010).

    Article  PubMed  Google Scholar 

  52. Weisstein, J.S., Goldsby, R.E. & O'Donnell, R.J. Oncologic approaches to pediatric limb preservation. J. Am. Acad. Orthop. Surg. 13, 544–554 (2005).

    Article  PubMed  Google Scholar 

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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.

Author information

Authors and Affiliations

Authors

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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