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Dynamics of motion signaling by neurons in macaque area MT

Abstract

Most neurons in macaque area MT are selective for the direction of stimulus motion. By comparing direction selectivity for gratings and plaids, we classified MT neurons as pattern direction selective (PDS) or component direction selective (CDS). We compared the time course of responses in CDS and PDS neurons in opiate-anesthetized macaques, using a rapid pseudorandom sequence of gratings and plaids that moved in different directions. On average, responses began 6 ms earlier in CDS neurons than in PDS neurons. More importantly, the pattern-selective responses of PDS neurons did not reach their fully selective state until 50–75 ms after the responses of CDS neurons had stabilized. The population motion response of MT is therefore initially dominated by component motion signals, and does not completely represent pattern motion until substantially later. The circuits that compute pattern motion take more time to finish their work than those signaling component motion.

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Figure 1: MT stimulus and response.
Figure 2: Three types of responses to plaids and gratings.
Figure 3: Pattern and component direction selectivity.
Figure 4: Response latency for pattern, component and unclassed cells.
Figure 5: Scatter plot of Z-scores over time in sliding or cumulative windows.
Figure 6: Line plots showing the evolution of Z-correlation values over time.

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References

  1. Celebrini, S., Thorpe, S., Trotter, Y. & Imbert, M. Dynamics of orientation coding in area V1 of the awake primate. Vis. Neurosci. 10, 811–825 (1993).

    Article  CAS  Google Scholar 

  2. Ringach, D.L., Hawken, M.J. & Shapley, R. The dynamics of orientation tuning in the macaque monkey striate cortex. Nature 387, 281–284 (1997).

    Article  CAS  Google Scholar 

  3. Ringach, D.L., Hawken, M.J. & Shapley, R. Dynamics of orientation tuning in macaque v1: the role of global and tuned suppression. J. Neurophysiol. 90, 342–352 (2003).

    Article  Google Scholar 

  4. Bair, W., Cavanaugh, J.R. & Movshon, J.A. Time course and time-distance relationships for surround suppression in macaque V1 neurons. J. Neurosci. 23, 7690–7701 (2003).

    Article  CAS  Google Scholar 

  5. Knierim, J.J. & Van Essen, D.C. Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J. Neurophysiol. 67, 961–980 (1992).

    Article  CAS  Google Scholar 

  6. Lee, T.S., Yang, C.F., Romero, R.D. & Mumford, D. Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency. Nat. Neurosci. 5, 589–597 (2002).

    Article  CAS  Google Scholar 

  7. Zipser, K., Lamme, V.A. & Schiller, P.H. Contextual modulation in primary visual cortex. J. Neurosci. 16, 7376–7389 (1996).

    Article  CAS  Google Scholar 

  8. Richmond, B.J., Optican, L.M., Podell, M. & Spitzer, H. Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. response characteristics. J. Neurophysiol. 57, 132–146 (1987).

    Article  CAS  Google Scholar 

  9. Richmond, B.J., Optican, L.M. & Spitzer, H. Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. I. Stimulus-response relations. J. Neurophysiol. 64, 351–369 (1990).

    Article  CAS  Google Scholar 

  10. Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869–873 (1999).

    Article  CAS  Google Scholar 

  11. Li, B., Chen, Y., Li, B.W., Wang, L.H. & Diao, Y.C. Pattern and component motion selectivity in cortical area PMLS of the cat. Eur. J. Neurosci. 14, 690–700 (2001).

    Article  CAS  Google Scholar 

  12. Pack, C.C. & Born, R.T. Two-dimensional substructure of MT receptive fields. Nature 409, 1040–1042 (2001).

    Article  CAS  Google Scholar 

  13. McClurkin, J.W., Optican, L.M., Richmond, B.J. & Gawne, T.J. Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science 253, 675–677 (1991).

    Article  CAS  Google Scholar 

  14. McLaughlin, D., Shapley, R., Shelley, M. & Wielaard, D.J. A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4cα . Proc. Natl. Acad. Sci. USA 97, 8087–8092 (2000).

    Article  CAS  Google Scholar 

  15. Bair, W., Koch, C., Newsome, W. & Britten, K. Power spectrum analysis of bursting cells in area MT in the behaving monkey. J. Neurosci. 14, 2870–2892 (1994).

    Article  CAS  Google Scholar 

  16. 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 

  17. Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. The analysis of visual moving patterns. in Pattern Recognition Mechanisms (eds. Chagas, C. Gattass, R. & Gross, C.) 117–151 (Springer, New York, 1985).

    Chapter  Google Scholar 

  18. Van Essen, D.C., Maunsell, J.H.R. & Bixby, J.L. The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization. J. Comp. Neurol. 199, 293–326 (1981).

    Article  CAS  Google Scholar 

  19. Zeki, S.M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol. (Lond.) 236, 549–573 (1974).

    Article  CAS  Google Scholar 

  20. Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992).

    Article  CAS  Google Scholar 

  21. Newsome, W.T. & Paré, E.B. A selective impairment of motion perception following lesions of the middle temporal area MT. J. Neurosci. 8, 2201–2211 (1988).

    Article  CAS  Google Scholar 

  22. DeValois, R.L., Albrecht, D.G. & Thorell, L.G. Spatial frequency selectivity of cells in macaque visual cortex. Vision Res. 22, 545–559 (1982).

    Article  CAS  Google Scholar 

  23. Movshon, J.A. & Newsome, W.T. Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741 (1996).

    Article  CAS  Google Scholar 

  24. Rodman, H.R. & Albright, T.D. Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Exp. Brain Res. 75, 53–64 (1989).

    Article  CAS  Google Scholar 

  25. Kooi, F.L., DeValois, K.K., Switkes, E. & Grosof, D.H. Higher-order factors influencing the perception of sliding and coherence of a plaid. Perception 21, 583–598 (1992).

    Article  CAS  Google Scholar 

  26. Lorenceau, J., Shiffrar, M., Wells, N. & Castet, E. Difference motion sensitive units are involved in recovering the direction of moving lines. Vision Res. 33, 1207–1217 (1993).

    Article  CAS  Google Scholar 

  27. Yo, C. & Wilson, H.R. Perceived direction of moving two-dimensional patterns depends on duration, contrast and eccentricity. Vision Res. 32, 135–147 (1992).

    Article  CAS  Google Scholar 

  28. Masson, G.S. & Castet, E. Parallel motion processing for the initiation of short-latency ocular following in humans. J. Neurosci. 22, 5149–5163 (2002).

    Article  CAS  Google Scholar 

  29. Stoner, G.R. & Albright, T.D. Neural correlates of perceptual motion coherence. Nature 358, 412–414 (1992).

    Article  CAS  Google Scholar 

  30. Priebe, N.J., Cassanello, C.R. & Lisberger, S.G. The neural representation of speed in macaque area MT/V5. J. Neurosci. 23, 5650–5661 (2003).

    Article  CAS  Google Scholar 

  31. Maunsell, J.H.R. Physiological evidence for two visual subsystems. in Matters of Intelligence (ed. L.M. Vaina) 59–87 (Reidel, Dordrecht, The Netherlands, 1987).

    Chapter  Google Scholar 

  32. Raiguel, S., Lagae, L., Gulyás, B. & Orban, G.A. Response latencies of visual cells in macaque areas V1, V2, and V5. Brain Res. 493, 155–159 (1989).

    Article  CAS  Google Scholar 

  33. 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 

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

    Article  CAS  Google Scholar 

  35. 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 

  36. Albrecht, D.G. Visual cortex neurons in monkey and cat: effect of contrast on the spatial and temporal phase transfer functions. Vis. Neurosci. 12, 1191–1210 (1995).

    Article  CAS  Google Scholar 

  37. Carandini, M., Heeger, D.J. & Movshon, J.A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621–8644 (1997).

    Article  CAS  Google Scholar 

  38. Gawne, T.J., Kjaer, T.W. & Richmond, B.J. Latency: another potential code for feature binding in striate cortex. J. Neurophysiol. 76, 1356–1360 (1996).

    Article  CAS  Google Scholar 

  39. Basole, A., White, L.E. & Fitzpatrick, D. Mapping multiple features in the population response of visual cortex. Nature 423, 986–990 (2003).

    Article  CAS  Google Scholar 

  40. Gizzi, M.S., Katz, E., Schumer, R.A. & Movshon, J.A. Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. J. Neurophysiol. 63, 1529–1543 (1990).

    Article  CAS  Google Scholar 

  41. Simoncelli, E.P. & Heeger, D.J. A model of neuronal responses in visual area MT. Vision Res. 38, 743–761 (1998).

    Article  CAS  Google Scholar 

  42. Albrecht, D.G., Geisler, W.S., Frazor, R.A. & Crane, A.M. Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. J. Neurophysiol. 88, 888–913 (2002).

    Article  Google Scholar 

  43. Bullier, J., Hupé, J.M., James, A.C. & Girard, P. The role of feedback connections in shaping the responses of visual cortical neurons. Prog. Brain Res. 134, 193–204 (2001).

    Article  CAS  Google Scholar 

  44. Wilson, H.R., Ferrera, V.P. & Yo, C. A psychophysically motivated model for two-dimensional motion perception. Vis. Neurosci. 9, 79–97 (1992).

    Article  CAS  Google Scholar 

  45. Gegenfurtner, K.R., Kiper, D.C. & Levitt, J.B. Functional properties of neurons in macaque area V3. J. Neurophysiol. 77, 1906–1923 (1997).

    Article  CAS  Google Scholar 

  46. Levitt, J.B., Kiper, D.C. & Movshon, J.A. Receptive fields and functional architecture of macaque V2. J. Neurophysiol. 71, 2517–2542 (1994).

    Article  CAS  Google Scholar 

  47. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  Google Scholar 

  48. Gallyas, F. Silver staining of myelin by means of physical development. Neurol. Res. 1, 203–209 (1979).

    Article  CAS  Google Scholar 

  49. Desimone, R. & Ungerleider, L.G. Multiple visual areas in the caudal superior temporal sulcus of the macaque. J. Comp. Neurol. 248, 164–189 (1986).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by a research grant from the NIH (EY02017), and by an HHMI Investigatorship to J.A.M. M.A.S. was supported in part by a National Eye Institute Institutional Training Grant (T32-7136). We thank A. Kohn, N. Rust and S. Schultz for assistance with some of the data collection, R. Young for technical assistance, and M. Hou and N. Doron for help with histology. We are grateful to W. Bair and A. Kohn for helpful advice and discussion.

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Smith, M., Majaj, N. & Movshon, J. Dynamics of motion signaling by neurons in macaque area MT. Nat Neurosci 8, 220–228 (2005). https://doi.org/10.1038/nn1382

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