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First spikes in ensembles of human tactile afferents code complex spatial fingertip events

Nature Neuroscience volume 7, pages 170–177 (2004)Cite this article

Abstract

It is generally assumed that primary sensory neurons transmit information by their firing rates. However, during natural object manipulations, tactile information from the fingertips is used faster than can be readily explained by rate codes. Here we show that the relative timing of the first impulses elicited in individual units of ensembles of afferents reliably conveys information about the direction of fingertip force and the shape of the surface contacting the fingertip. The sequence in which different afferents initially discharge in response to mechanical fingertip events provides information about these events faster than the fastest possible rate code and fast enough to account for the use of tactile signals in natural manipulation.

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Figure 1: Force stimulation, afferent sample and responses to fingertip forces applied in different directions with the flat surface.
Figure 2: Afferents' directional sensitivity in the tangential plane.
Figure 3: Discrimination of force direction by FA-I, SA-I and SA-II afferents based on the relative timing of first spikes and on first-interspike intervals.
Figure 4: Discrimination of shape of stimulus surface by FA-I, SA-I and SA-II afferents based on the relative timing of the first spikes evoked in ensembles of tactile afferents and on the first-interspike intervals.
Figure 5: Effect of shape of stimulus surface on first-spike latencies of afferents responding to normal force stimulation with both the flat and the most curved surface (200 m−1).

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References

  1. Adrian, E.D. The Basis of Sensation (W.W. Norton, New York, 1928).

    Google Scholar 

  2. Johansson, R.S. & Westling, G. Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp. Brain Res. 56, 550–564 (1984).

    Article  CAS  Google Scholar 

  3. Johansson, R.S. & Westling, G. Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp. Brain Res. 66, 141–154 (1987).

    Article  CAS  Google Scholar 

  4. Jenmalm, P. & Johansson, R.S. Visual and somatosensory information about object shape control manipulative finger tip forces. J. Neurosci. 17, 4486–4499 (1997).

    Article  CAS  Google Scholar 

  5. Johansson, R.S., Häger, C. & Riso, R. Somatosensory control of precision grip during unpredictable pulling loads. II. Changes in load force rate. Exp. Brain Res. 89, 192–203 (1992).

    Article  CAS  Google Scholar 

  6. Häger-Ross, C., Cole, K.J. & Johansson, R.S. Grip force responses to unanticipated object loading: Load direction reveals body- and gravity-referenced intrinsic task variables. Exp. Brain Res. 110, 142–150 (1996).

    PubMed  Google Scholar 

  7. Macefield, V.G., Hager Ross, C. & Johansson, R.S. Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp. Brain Res. 108, 155–171 (1996).

    CAS  PubMed  Google Scholar 

  8. Johansson, R.S., Lemon, R.N. & Westling, G. Time varying enhancement of human cortical excitability mediated by cutaneous inputs during precision grip. J. Physiol. (Lond.) 481, 761–775 (1994).

    Article  CAS  Google Scholar 

  9. Rolls, E.T. & Tovee, M.J. Processing speed in the cerebral cortex and the neurophysiology of visual masking. Proc. R. Soc. Lond. B Biol. Sci. 257, 9–15 (1994).

    Article  CAS  Google Scholar 

  10. Nielsen, J., Petersen, N. & Fedirchuk, B. Evidence suggesting a transcortical pathway from cutaneous foot afferents to tibialis anterior motoneurones in man. J. Physiol. (Lond.) 501, 473–484 (1997).

    Article  CAS  Google Scholar 

  11. Westling, G. & Johansson, R.S. Responses in glabrous skin mechanoreceptors during precision grip in humans. Exp. Brain Res. 66, 128–140 (1987).

    Article  CAS  Google Scholar 

  12. Thorpe, S., Delorme, A. & Van Rullen, R. Spike-based strategies for rapid processing. Neural Net. 14, 715–725 (2001).

    Article  CAS  Google Scholar 

  13. Birznieks, I., Jenmalm, P., Goodwin, A. & Johansson, R. Encoding of direction of fingertip forces by human tactile afferents. J. Neurosci. 21, 8222–8237 (2001).

    Article  CAS  Google Scholar 

  14. Jenmalm, P., Birznieks, I., Goodwin, A.W. & Johansson, R.S. Influence of object shape on responses of human tactile afferents under conditions characteristic of manipulation. Eur. J. Neurosci. 18, 164–176 (2003).

    Article  Google Scholar 

  15. Vallbo, A.B. & Hagbarth, K.E. Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. Exp. Neurol. 21, 270–289 (1968).

    Article  CAS  Google Scholar 

  16. Johansson, R.S. & Vallbo, Å.B. Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci. 6, 27–31 (1983).

    Article  Google Scholar 

  17. Johansson, R.S. Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J. Physiol. (Lond.) 281, 101–125 (1978).

    Article  CAS  Google Scholar 

  18. Johansson, R.S. & Vallbo, A.B. Spatial properties of the population of mechanoreceptive units in the glabrous skin of the human hand. Brain Res. 184, 353–366 (1980).

    Article  CAS  Google Scholar 

  19. Johansson, R.S. & Vallbo, A.B. Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand. J. Physiol. (Lond.) 0297, 405–422 (1979).

    Article  CAS  Google Scholar 

  20. Goodwin, A.W., Browning, A.S. & Wheat, H.E. Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad. J. Neurosci. 15, 798–810 (1995).

    Article  CAS  Google Scholar 

  21. Maeno, T., Kobay-Ashi, K. & Yamazaki, N. Relationship between the structure of human finger tissue and the location of tactile receptors. JSME Int. J. 41, 94–100 (1998).

    Article  Google Scholar 

  22. Pawluk, D.T. & Howe, R.D. Dynamic lumped element response of the human fingerpad. J. Biomech. Eng. 121, 178–183 (1999).

    Article  CAS  Google Scholar 

  23. Nakazawa, N., Ikeura, R. & Inooka, H. Characteristics of human fingertips in the shearing direction. Biol. Cybern. 82, 207–214 (2000).

    Article  CAS  Google Scholar 

  24. Johansson, R.S. & Vallbo, A.B. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J. Physiol. (Lond.) 286, 283–300 (1979).

    Article  CAS  Google Scholar 

  25. Phillips, J.R., Johansson, R.S. & Johnson, K.O. Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin. J. Neurosci. 12, 827–839 (1992).

    Article  CAS  Google Scholar 

  26. Trulsson, M. & Essick, G.K. Low-threshold mechanoreceptive afferents in the human lingual nerve. J. Neurophysiol. 77, 737–748 (1997).

    Article  CAS  Google Scholar 

  27. Kennedy, P.M. & Inglis, J.T. Distribution and behaviour of glabrous cutaneous receptors in the human foot sole. J. Physiol. (Lond.) 538, 995–1002 (2002).

    Article  CAS  Google Scholar 

  28. Johansson, R.S. & Cole, K.J. Sensory-motor coordination during grasping and manipulative actions. Curr. Opin. Neurobiol. 2, 815–823 (1992).

    Article  CAS  Google Scholar 

  29. Johansson, R.S. Sensory input and control of grip. in Sensory Guidance of Movement. Novartis Foundation Symposium 218. 45–59 (Wiley & Sons, Chichester, 1998).

    Google Scholar 

  30. Johansson, R.S., Landström, U. & Lundström, R. Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements. Brain Res. 244, 17–25 (1982).

    Article  CAS  Google Scholar 

  31. Pubols, B.H. Jr. Factors affecting cutaneous mechanoreceptor response: II. Changes in mechanical properties of skin with repeated stimulation. J. Neurophysiol. 47, 530–542 (1982).

    Article  Google Scholar 

  32. Panzeri, S., Petersen, R.S., Schultz, S.R., Lebedev, M. & Diamond, M.E. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29, 769–777 (2001).

    Article  CAS  Google Scholar 

  33. Petersen, R.S., Panzeri, S. & Diamond, M.E. Population coding of stimulus location in rat somatosensory cortex. Neuron 32, 503–514 (2001).

    Article  CAS  Google Scholar 

  34. Rowe, M.J. Synaptic transmission between single tactile and kinaesthetic sensory nerve fibers and their central target neurones. Behav. Brain Res. 135, 197–212 (2002).

    Article  Google Scholar 

  35. Usrey, W.M. The role of spike timing for thalamocortical processing. Curr. Opin. Neurobiol. 12, 411–417 (2002).

    Article  CAS  Google Scholar 

  36. Meister, M. & Berry, M.J. The neural code of the retina. Neuron 22, 435–450 (1999).

    Article  CAS  Google Scholar 

  37. Reich, D.S., Mechler, F. & Victor, J.D. Temporal coding of contrast in primary visual cortex: when, what and why. J. Neurophysiol. 85, 1039–1050 (2001).

    Article  CAS  Google Scholar 

  38. Gerstner, W. & Kistler, W.M. Spiking Neuron Models (Cambridge Univ. Press, Cambridge, 2002).

  39. Johansson, R.S., Westling, G., Bäckström, A. & Flanagan, J.R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001).

    Article  CAS  Google Scholar 

  40. Sommer, M.A. & Wurtz, R.H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002).

    Article  CAS  Google Scholar 

  41. Harris, F., Jabbur, S.J., Morse, R.W. & Tow, A.L. Influence of the cerebral cortex on the cuneate nucleus of the monkey. Nature 208, 1215–1216 (1965).

    Article  CAS  Google Scholar 

  42. Adkins, R.J., Morse, R.W. & Towe, A.L. Control of somatosensory input by cerebral cortex. Science 153, 1020–1022 (1966).

    Article  CAS  Google Scholar 

  43. Ergenzinger, E.R., Glasier, M.M., Hahm, J.O. & Pons, T.P. Cortically induced thalamic plasticity in the primate somatosensory system. Nat. Neurosci. 1, 226–229 (1998).

    Article  CAS  Google Scholar 

  44. Engel, A.K., Fries, P. & Singer, W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2, 704–716 (2001).

    Article  CAS  Google Scholar 

  45. Hopfield, J.J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36 (1995).

    Article  CAS  Google Scholar 

  46. Carr, C.E. Processing of temporal information in the brain. Annu. Rev. Neurosci. 16, 223–243 (1993).

    Article  CAS  Google Scholar 

  47. Kakuda, N. Conduction velocity of low-threshold mechanoreceptive afferent fibers in the glabrous and hairy skin of human hands measured with microneurography and spike-triggered averaging. Neurosci. Res. 15, 179–188 (1992).

    Article  CAS  Google Scholar 

  48. Zar, J.H. Biostatistical Analysis (Prentice-Hall, Upper Saddle River, New Jersey, USA 1996).

    Google Scholar 

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Acknowledgements

We thank G. Westling, L. Bäckström and M. Andersson for technical support, and A. Goodwin and P. Jenmalm for their contributions during the experiments. This work was supported by the Swedish Medical Research Council (project 08667), J.C. Kempe's Memorial Foundation and the 5th Framework Program of the EU (project IST-2001-33073).

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  1. Department of Integrative Medical Biology, Physiology Section, Umeå University, SE-901 87, Umeå, Sweden

    Roland S Johansson & Ingvars Birznieks

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Correspondence to Roland S Johansson.

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Johansson, R., Birznieks, I. First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7, 170–177 (2004). https://doi.org/10.1038/nn1177

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