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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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).
Ringach, D.L., Hawken, M.J. & Shapley, R. The dynamics of orientation tuning in the macaque monkey striate cortex. Nature 387, 281–284 (1997).
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).
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).
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).
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).
Zipser, K., Lamme, V.A. & Schiller, P.H. Contextual modulation in primary visual cortex. J. Neurosci. 16, 7376–7389 (1996).
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).
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).
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).
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).
Pack, C.C. & Born, R.T. Two-dimensional substructure of MT receptive fields. Nature 409, 1040–1042 (2001).
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).
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).
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).
Albright, T.D. Direction and orientation selectivity of neurons in visual area MT of the macaque. J. Neurophysiol. 52, 1106–1130 (1984).
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).
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).
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).
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).
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).
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. Spatial frequency selectivity of cells in macaque visual cortex. Vision Res. 22, 545–559 (1982).
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).
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).
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).
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).
Yo, C. & Wilson, H.R. Perceived direction of moving two-dimensional patterns depends on duration, contrast and eccentricity. Vision Res. 32, 135–147 (1992).
Masson, G.S. & Castet, E. Parallel motion processing for the initiation of short-latency ocular following in humans. J. Neurosci. 22, 5149–5163 (2002).
Stoner, G.R. & Albright, T.D. Neural correlates of perceptual motion coherence. Nature 358, 412–414 (1992).
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).
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).
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).
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).
Schmolesky, M.T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).
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).
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).
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).
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).
Basole, A., White, L.E. & Fitzpatrick, D. Mapping multiple features in the population response of visual cortex. Nature 423, 986–990 (2003).
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).
Simoncelli, E.P. & Heeger, D.J. A model of neuronal responses in visual area MT. Vision Res. 38, 743–761 (1998).
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).
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).
Wilson, H.R., Ferrera, V.P. & Yo, C. A psychophysically motivated model for two-dimensional motion perception. Vis. Neurosci. 9, 79–97 (1992).
Gegenfurtner, K.R., Kiper, D.C. & Levitt, J.B. Functional properties of neurons in macaque area V3. J. Neurophysiol. 77, 1906–1923 (1997).
Levitt, J.B., Kiper, D.C. & Movshon, J.A. Receptive fields and functional architecture of macaque V2. J. Neurophysiol. 71, 2517–2542 (1994).
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).
Gallyas, F. Silver staining of myelin by means of physical development. Neurol. Res. 1, 203–209 (1979).
Desimone, R. & Ungerleider, L.G. Multiple visual areas in the caudal superior temporal sulcus of the macaque. J. Comp. Neurol. 248, 164–189 (1986).
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.
The authors declare no competing financial interests.
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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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