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Instructive signals for motor learning from visual cortical area MT

An Erratum to this article was published on 01 July 2005

Abstract

Sensory error signals have long been proposed to act as instructive signals to guide motor learning. Here we have exploited the temporal specificity of learning in smooth pursuit eye movements and the well-defined anatomical structure of the neural circuit for pursuit to identify a part of sensory cortex that provides instructive signals for motor learning in monkeys. We show that electrical microstimulation in the motion-sensitive middle temporal area (MT) of extrastriate visual cortex instructs learning in smooth eye movements in a way that closely mimics the learning instructed by real visual motion. We conclude that MT provides instructive signals for motor learning in smooth pursuit eye movements under natural conditions, suggesting a similar role for sensory cortices in many kinds of learned behaviors.

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Figure 1: A sample experiment using MT microstimulation to instruct learning.
Figure 2: Summary of learned eye velocity when stimulation in MT provided the instructive signal for learning.
Figure 3: Summary of learned eye velocity when stimulation in MT combined with target stabilization provided the instructive signal for learning.
Figure 4: Learning instructed by motion of a visual background during orthogonal target motion.
Figure 5: Temporal relationship between learning instructed by MT microstimulation and visual background motion.
Figure 6: Comparison of learning instructed by MT stimulation and visual background motion at different times after the onset of pursuit target motion.

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References

  1. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    Article  CAS  Google Scholar 

  2. Rescorla, R.A. & Wagner, A.R. A theory of pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. in Classical Conditioning II: Current Research and Theory (eds. Black, A.H. & Prokasy, W.F.) 64–99 (Appleton Century Crofts, New York, 1972).

    Google Scholar 

  3. Ito, M. Neural design of the cerebellar motor control system. Brain Res. 40, 81–84 (1972).

    Article  CAS  Google Scholar 

  4. Rashbass, C. The relationship between saccadic and smooth tracking eye movements. J. Physiol. (Lond.) 159, 326–338 (1961).

    Article  CAS  Google Scholar 

  5. Robinson, D.A. The mechanics of human smooth pursuit eye movement. J. Physiol. (Lond.) 180, 569–591 (1965).

    Article  CAS  Google Scholar 

  6. Kahlon, M. & Lisberger, S.G. Coordinate system for learning in the smooth pursuit eye movements of monkeys. J. Neurosci. 16, 7270–7283 (1996).

    Article  CAS  Google Scholar 

  7. Medina, J.F., Carey, M.R. & Lisberger, S.G. The representation of time for motor learning. Neuron 45, 157–167 (2005).

    Article  CAS  Google Scholar 

  8. Boman, D.K. & Hotson, J.R. Predictive smooth pursuit eye movements near abrupt changes in motion direction. Vision Res. 32, 675–689 (1992).

    Article  CAS  Google Scholar 

  9. Maunsell, J.H. & Van Essen, D.C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J. Neurophysiol. 49, 1127–1147 (1983).

    Article  CAS  Google Scholar 

  10. Albright, T.D. Direction and orientation selectivity of neurons in visual area MT of the macaque. J. Neurophysiol. 52, 1106–1130 (1984).

    Article  CAS  Google Scholar 

  11. Newsome, W.T., Wurtz, R.H., Dursteler, M.R. & Mikami, A. Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. J. Neurosci. 5, 825–840 (1985).

    Article  CAS  Google Scholar 

  12. Newsome, W.T., Wurtz, R.H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements II. Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–620 (1988).

    Article  CAS  Google Scholar 

  13. Lisberger, S.G. & Movshon, J.A. Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J. Neurosci. 19, 2224–2246 (1999).

    Article  CAS  Google Scholar 

  14. Komatsu, H. & Wurtz, R.H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophysiol. 62, 31–47 (1989).

    Article  CAS  Google Scholar 

  15. Groh, J.M., Born, R.T. & Newsome, W.T. How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J. Neurosci. 17, 4312–4330 (1997).

    Article  CAS  Google Scholar 

  16. Salzman, C.D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).

    Article  CAS  Google Scholar 

  17. Bisley, J.W., Zaksas, D. & Pasternak, T. Microstimulation of cortical area MT affects performance on a visual working memory task. J. Neurophysiol. 85, 187–196 (2001).

    Article  CAS  Google Scholar 

  18. Kodaka, Y., Miura, K., Suehiro, K., Takemura, A. & Kawano, K. Ocular tracking of moving targets: effects of perturbing the background. J. Neurophysiol. 91, 2474–2483 (2004).

    Article  Google Scholar 

  19. Schmolesky, M.T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).

    Article  CAS  Google Scholar 

  20. Raiguel, S.E., Xiao, D.K., Marcar, V.L. & Orban, G.A. Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. J. Neurophysiol. 82, 1944–1956 (1999).

    Article  CAS  Google Scholar 

  21. Cook, E.P. & Maunsell, J.H. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat. Neurosci. 5, 985–994 (2002).

    Article  CAS  Google Scholar 

  22. Bair, W., Cavanaugh, J.R., Smith, M.A. & Movshon, J.A. The timing of response onset and offset in macaque visual neurons. J. Neurosci. 22, 3189–3205 (2002).

    Article  CAS  Google Scholar 

  23. Mauk, M.D., Steinmetz, J.E. & Thompson, R.F. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc. Natl. Acad. Sci. USA 83, 5349–5353 (1986).

    Article  CAS  Google Scholar 

  24. Talwar, S.K. & Gerstein, G.L. Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior. J. Neurophysiol. 86, 1555–1572 (2001).

    Article  CAS  Google Scholar 

  25. Kowler, E. Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Vision Res. 29, 1049–1057 (1989).

    Article  CAS  Google Scholar 

  26. Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003).

    Article  CAS  Google Scholar 

  27. Chou, I.H. & Lisberger, S.G. The role of the frontal pursuit area in learning in smooth pursuit eye movements. J. Neurosci. 24, 4124–4133 (2004).

    Article  CAS  Google Scholar 

  28. Kahlon, M. & Lisberger, S.G. Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J. Neurophysiol. 84, 2945–2960 (2000).

    Article  CAS  Google Scholar 

  29. Distler, C., Mustari, M.J. & Hoffmann, K.P. Cortical projections to the nucleus of the optic tract and dorsal terminal nucleus and to the dorsolateral pontine nucleus in macaques: a dual retrograde tracing study. J. Comp. Neurol. 444, 144–158 (2002).

    Article  Google Scholar 

  30. Alley, K., Baker, R. & Simpson, J.I. Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit. Brain Res. 98, 582–589 (1975).

    Article  CAS  Google Scholar 

  31. Brodal, P. The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193–208 (1979).

    Article  CAS  Google Scholar 

  32. Raymond, J.L. & Lisberger, S.G. Neural learning rules for the vestibulo-ocular reflex. J. Neurosci. 18, 9112–9129 (1998).

    Article  CAS  Google Scholar 

  33. Medina, J.F., Nores, W.L., Ohyama, T. & Mauk, M.D. Mechanisms of cerebellar learning suggested by eyelid conditioning. Curr. Opin. Neurobiol. 10, 717–724 (2000).

    Article  CAS  Google Scholar 

  34. Bell, C.C., Han, V.Z., Sugawara, Y. & Grant, K. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387, 278–281 (1997).

    Article  CAS  Google Scholar 

  35. Wang, S.S., Denk, W. & Hausser, M. Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3, 1266–1273 (2000).

    Article  CAS  Google Scholar 

  36. Chen, C. & Thompson, R.F. Temporal specificity of long-term depression in parallel fiber–Purkinje synapses in rat cerebellar slice. Learn. Mem. 2, 185–198 (1995).

    Article  CAS  Google Scholar 

  37. Brenowitz, S.D. & Regehr, W.G. Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45, 419–431 (2005).

    Article  CAS  Google Scholar 

  38. Middleton, F.A. & Strick, P.L. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Brain Res. Rev. 31, 236–250 (2000).

    Article  CAS  Google Scholar 

  39. Tian, J.R. & Lynch, J.C. Subcortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkey. J. Neurosci. 17, 9233–9247 (1997).

    Article  CAS  Google Scholar 

  40. Doya, K. Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr. Opin. Neurobiol. 10, 732–739 (2000).

    Article  CAS  Google Scholar 

  41. Hikosaka, O., Nakamura, K., Sakai, K. & Nakahara, H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222 (2002).

    Article  CAS  Google Scholar 

  42. Jueptner, M., Frith, C.D., Brooks, D.J., Frackowiak, R.S. & Passingham, R.E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 77, 1325–1337 (1997).

    Article  CAS  Google Scholar 

  43. Carey, M.R. & Lisberger, S.G. Signals that modulate gain control for smooth pursuit eye movements in monkeys. J. Neurophysiol. 91, 623–631 (2004).

    Article  Google Scholar 

  44. Churchland, M.M. & Lisberger, S.G. Shifts in the population response in the middle temporal visual area parallel perceptual and motor illusions produced by apparent motion. J. Neurosci. 21, 9387–9402 (2001).

    Article  CAS  Google Scholar 

  45. Morris, E.J. & Lisberger, S.G. Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. J. Neurophysiol. 58, 1351–1369 (1987).

    Article  CAS  Google Scholar 

  46. Murasugi, C.M., Salzman, C.D. & Newsome, W.T. Microstimulation in visual area MT: effects of varying pulse amplitude and frequency. J. Neurosci. 13, 1719–1729 (1993).

    Article  CAS  Google Scholar 

  47. Born, R.T., Groh, J.M., Zhao, R. & Lukasewycz, S.J. Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements. Neuron 26, 725–734 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Brainard, D. Copenhagen, M. Mauk, W. Newsome, M. Orger, R. Ramachandran, P. Sabes and D. Bodznick for helpful discussion; L. Bocskai, D. Kleinhesselink, K. McGary, S. Ruffner and D. Wolfgang-Kimball for excellent technical support and S. Tokiyama, E. Montgomery, B. St. Amant and K. MacLeod for superb animal care. This work was supported by the Howard Hughes Medical Institute, US National Institutes of Health grant NS34835, and an Achievement Rewards for College Scientists fellowship to M.R.C.

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Correspondence to Megan R Carey.

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Supplementary information

Supplementary Fig. 1

Quantitative analysis of possible correlations between the amplitude of the learned eye movement and response properties of neurons at each stimulation site. (PDF 199 kb)

Supplementary Fig. 2

Distribution of learned eye velocities across experiments or trials when learning was instructed by MT stimulation without or with target stabilization. (PDF 836 kb)

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Carey, M., Medina, J. & Lisberger, S. Instructive signals for motor learning from visual cortical area MT. Nat Neurosci 8, 813–819 (2005). https://doi.org/10.1038/nn1470

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