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Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl

Abstract

TO generate behaviour, the brain must transform sensory information into signals that are appropriate to control movement. Sensory and motor coordinate frames are fundamentally different, however: sensory coordinates are based on the spatiotemporal patterns of activity arising from the various sense organs, whereas motor coordinates are based on the pulling directions of muscles or groups of muscles. Results from psychophysical experiments suggest that in the process of transforming sensory information into motor control signals, the brain encodes movements in abstract or extrinsic coordinate frames1–5, that is ones not closely related to the geometry of the sensory apparatus or of the skeletomusculature. Here we show that an abstract code underlies movements of the head by the barn owl. Specifically, the data show that subsequent to the retinotopic code for space in the optic tectum yet before the motor neuron code for muscle tensions there exists a code for head movement in which upward, downward, leftward and rightward components of movement are controlled by four functionally distinct neural circuits. Such independent coding of orthogonal components of movement may be a common intermediate step in the transformation of sensation into behaviour.

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References

  1. Bernstein, N. The Co-ordination and Regulation of Movements (Pergamon, Oxford, 1967).

    Google Scholar 

  2. Hollerbach, J. M. & Flash, T. Biol. Cybern. 44, 67–77 (1982).

    Article  CAS  Google Scholar 

  3. Morasso, P. Expl. Brain Res. 42, 223–237 (1981).

    Article  ADS  CAS  Google Scholar 

  4. Bizzi, E., Accornero, N., Chapple, W. & Hogan, N. J. Neurosci. 4, 2738–2744 (1984).

    Article  CAS  Google Scholar 

  5. Soechting, J. F. & Flanders M. J. Neurophysiol. 62, 595–608 (1989).

    Article  CAS  Google Scholar 

  6. Syka, J. & Radil-Weiss, T. Brain Res. 28, 567–572 (1971).

    Article  CAS  Google Scholar 

  7. Ewert, J.-P. Brain Behav. Evol. 3, 36–56 (1970).

    Article  CAS  Google Scholar 

  8. Schiller, P. J. & Stryker, M. J. Neurophysiol. 35, 915–924 (1972).

    Article  CAS  Google Scholar 

  9. Wurtz, R. H. & Goldberg, M. E. Science 171, 82–84 (1971).

    Article  ADS  CAS  Google Scholar 

  10. Sparks, D. L. Brain Res. 156, 1–16 (1978).

    Article  ADS  CAS  Google Scholar 

  11. du Lac, S. & Knudsen, E. I. J. Neurophysiol. 63, 131–146 (1989).

    Article  Google Scholar 

  12. Robinson, D. Vis. Res. 12, 1795–1808 (1972).

    Article  CAS  Google Scholar 

  13. Masino, T. & Knudsen, E. I. Soc. Neurosci. Abstr. 14, 1236 (1988).

    Google Scholar 

  14. Masino, T. & Grobstein, P. J. comp. Neurol. 291, 103–127 (1990).

    Article  CAS  Google Scholar 

  15. Grantyn, A. & Berthoz, A. in Control of Head Movement (eds Peterson B. & Richmond, F.J.) 224–244 (Oxford University Press, 1988).

    Google Scholar 

  16. Fukushima, K. Prog. Neurobiol. 29, 107–192 (1987).

    Article  CAS  Google Scholar 

  17. Westheimer, G. & Blair, S. M. Expl Brain Res. 24, 89–95 (1975).

    Article  CAS  Google Scholar 

  18. Soechting, J. F. & Ross, B. Neuroscience 13, 595–604 (1984).

    Article  CAS  Google Scholar 

  19. Lacquaniti, F. Trends Neurosci. 12; 287–291 (1989).

    Article  CAS  Google Scholar 

  20. Kostyk, S. K. & Grobstein, P. Neuroscience 21; 41–55 (1987).

    Article  CAS  Google Scholar 

  21. Grobstein, P. Brain Behav. Evol. 31, 34–48 (1988).

    Article  CAS  Google Scholar 

  22. Masino, T. & Grobstein, P. Expl. Brain Res. 75, 227–244 (1989).

    Article  CAS  Google Scholar 

  23. Masino, T. & Grobstein, P. Expl. Brain Res. 75, 245–264 (1989).

    Article  CAS  Google Scholar 

  24. Knudsen, E. I., du Lac, S. & Esterly, S. A. Rev. Neurosci. 10, 41–65 (1987).

    Article  CAS  Google Scholar 

  25. Simpson, J. I. & Graf, W. Rev. Oculomotor Res. 1, 3–20 (1985).

    Google Scholar 

  26. Grobstein, P. Visuomotor Coordination (eds Ewert, J.-P. & Arbib, M. A.) 537–568 (Plenum, New York, 1989).

    Book  Google Scholar 

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Masino, T., Knudsen, E. Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl. Nature 345, 434–437 (1990). https://doi.org/10.1038/345434a0

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