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Processing of first-order motion in marmoset visual cortex is influenced by second-order motion


We measured the responses of single neurons in marmoset visual cortex (V1, V2, and the third visual complex) to moving first-order stimuli and to combined first- and second-order stimuli in order to determine whether first-order motion processing was influenced by second-order motion. Beat stimuli were made by summing two gratings of similar spatial frequency, one of which was static and the other was moving. The beat is the product of a moving sinusoidal carrier (first-order motion) and a moving low-frequency contrast envelope (second-order motion). We compared responses to moving first-order gratings alone with responses to beat patterns with first-order and second-order motion in the same direction as each other, or in opposite directions to each other in order to distinguish first-order and second-order direction-selective responses. In the majority (72%, 67/93) of cells (V1 73%, 45/62; V2 70%, 16/23; third visual complex 75%, 6/8), responses to first-order motion were significantly influenced by the addition of a second-order signal. The second-order envelope was more influential when moving in the opposite direction to the first-order stimulus, reducing first-order direction sensitivity in V1, V2, and the third visual complex. We interpret these results as showing that first-order motion processing through early visual cortex is not separate from second-order motion processing; suggesting that both motion signals are processed by the same system.

Corresponding author
Address correspondence and reprint requests to: Nick Barraclough, University of Hull, Department of Psychology, East Yorkshire HU6 7RX, United Kingdom. E-mail:
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Albrecht, D.G. & De Valois, R.L. (1981). Striate cortex responses to periodic patterns with and without the fundamental harmonics. Journal of Physiology 319, 497514.
Badcock, D.-R. & Derrington, A.-M. (1985). Detecting the displacement of periodic patterns. Vision Research 25, 12531258.
Bourne, J.A., Lui, L., Tweedale, R., & Rosa, M.G.P. (2004). First- and second-order stimulus length selectivity in new world monkey striate cortex. European Journal of Neuroscience 19, 169180.
Bourne, J.A., Tweedale, R., & Rosa, M.G.P. (2002). Physiological responses of new world monkey V1 neurons to stimuli defined by coherent motion. Cerebral Cortex 12, 11321145.
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103129.
Chaudhuri, A. & Albright, T.D. (1997). Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1. Visual Neuroscience 14, 949962.
Chubb, C. & Sperling, G. (1988). Drift-balanced random stimuli: A general basis for studying non-Fourier motion perception. Journal of the Optical Society of America A 5, 19862007.
Clifford, C.W.G. & Vaina, L.M. (1999). A computational model of selective deficits in first and second-order motion processing. Vision Research 39, 113130.
Derrington, A.M. & Badcock, D.R. (1985). Separate detectors for simple and complex grating patterns? Vision Research 25, 18691878.
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219240.
Edwards, M. & Nishida, S. (2004). Contrast-reversing global-motion stimuli reveal local interactions between first- and second-order motion signals. Vision Research 44, 19411950.
Felisberti, F. & Derrington, A.M. (2001). Long-range interactions in the lateral geniculate nucleus of the New-World monkey, Callithrix jacchus. Visual Neuroscience 18, 209218.
Greenlee, M.W. & Smith, A.T. (1997). Detection and discrimination of first and second-order motion in patients with unilateral brain damage. Journal of Neuroscience 17, 804818.
Harris, L.R. & Smith, A.T. (1992). Motion defined by second-order characteristics does not evoke optokinectic nystagmus. Visual Neuroscience 9, 565570.
Johnston, A., McOwan, P.W., & Buxton, H. (1992). A computational model of the analysis of some first-order and second-order motion patterns by simple and complex cells. Proceedings of the Royal Society of London B 250, 297306.
Johnston, A. & Clifford, C.W.G. (1995). Perceived motion of contrast-modulated gratings: Prediction of the multi-channel gradient model and the role of full-wave rectification. Vision Research 35, 17711783.
Kaske, A., Dick, A., & Creutzfeldt, O.D. (1991). The local domain for divergence of subcortical afferents to the striate and extrastriate visual cortex in the common marmoset (Callithrix jacchus): a multiple labeling study. Experimental brain research 84, 254265.
Ledgeway, T. & Smith, A.T. (1994). Evidence for separate motion-detecting mechanisms for first- and second-order motion in human vision. Vision Research 34, 27272740.
Lee, C., Weyand, T.G., & Malpeli, J.G. (1998). Thalamic control of cat area-18 supragranular layers: Simple cells, complex cells, and cells projecting to the lateral suprasylvian visual area. Visual Neuroscience 15, 2735.
LeVay, S. & Gilbert, C.D. (1976). Laminar patterns of geniculocortical projection in the cat. Brain Research 113, 119.
Levitt, J.B., Lund, J.S., & Yoshioka, T. (1996). Anatomical substrates for early stages in cortical processing of visual information in the macaque monkey. Behavioural Brain Research 76, 519.
Lu, Z.-L. & Sperling, G. (1995). The functional architecture of human visual motion perception. Vision Research 35, 26972722.
Lyon, D.C. & Kaas, J.H. (2001). Connectional and architectonic evidence for dorsal and ventral and dorsomedial area in marmoset monkeys. Journal of Neuroscience 21, 249261.
Mareschal, I. & Baker, C.L. (1998a). A cortical locus for the processing of contrast-defined contours. Nature Neuroscience 1, 150154.
Mareschal, I. & Baker, C.L. (1998b). Temporal and spatial response to second-order stimuli in cat area 18. Journal of Neurophysiology 80, 28112823.
Mather, G. & West, S. (1993). Evidence for second-order motion detectors. Vision Research 33, 11091112.
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrode. Medical and Biological Engineering 10, 495504.
Movshon, J.A. & Newsome, W.T. (1996). Visual response properties of striate cortical neurons projecting to area MT in macaque. Journal of Neuroscience 16, 77337741.
Nishida, S., Ledgeway, T., & Edwards, M. (1997). Dual multiple-scale processing for motion in the human visual system. Vision Research 37, 26852698.
Nishida, S., Sasaki, Y., Murakami, I., Watanabe, T., & Tootell, B.H. (2003). Neuroimaging of direction-selective mechanisms for second-order motion. Journal of Neurophysiology 90, 32423254.
Pessoa, V.F., Abrahao, J.C.H., Pacheco, R.A., Pereira, L.C.M., Magalhaes-Castro, B., & Saraiva, P.E.S. (1992). Relative sizes of cortical visual areas in marmosets: Functional and phylogenetic implications. Experimental Brain Research 88, 459462.
Rosa, M.G.P., Fritsches, K.A., & Elston, G.N. (1997). The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity. Journal of Comparative Neurology 387, 547567.
Rosa, M.G.P. & Manger, P.R. (2005). Clarifying homologies in the mammalian cerebral cortex: The case of the third visual area (V3). Clinical and Experimental Pharmacology and Physiology 32, 327339.
Rosa, M.G.P., Palmer, S.M., Gamberini, M., Tweedale, R., Pinon, M.C., & Bourne, J.A. (2005). Resolving the organization of the new world monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus). Journal of Comparative Neurology 483, 164191.
Scott-Samuel, N.E. & Georgeson, M.A. (1999). Does early non-linearity account for second-order motion? Vision Research 39, 28532865.
Sofue, A., Kaneoke, Y., & Kakigi, R. (2003). Physiological evidence of interaction of first- and second-order motion processes in the human visual system: A magnetoencephalographic study. Human Brain Mapping 20, 158167.
Taub, E., Victor, J.D., & Conte, M.M. (1997). Nonlinear preprocessing in short-range motion. Vision Research 37, 14591477.
Vaina, L.M. & Cowey, A. (1996). Impairment of the perception of second order motion but not first order motion in a patient with unilateral focal brain damage. Proceedings of the Royal Society of London B 263, 12251232.
Webb, B.S., Tinsley, C.J., Barraclough, N.E., Easton, A., Parker, A., & Derrington, A.M. (2002). Feedback from V1 and inhibition from beyond the classical receptive field modulates the responses of neurons in the primate lateral geniculate nucleus. Visual Neuroscience 19, 110.
Wilson, H.R., Ferrera, V.P., & Yo, C. (1992). A psychophysical motivated model for two-dimensional motion perception. Visual Neuroscience 9, 7997.
Zeki, S. (1990). The motion pathways of the visual cortex. In Vision: Coding and efficiency, ed. Blakemore, C., pp. 321345. Cambridge, UK: Cambridge University Press.
Zhou, Y.X. & Baker, C.L. (1993). A processing stream in mammalian visual cortex neurons for non-fourier responses. Science 261, 98101.
Zhou, Y.X. & Baker, C.L. (1994). Envelope-responsive neurons in areas 17 and 18 of cat. Journal of Neurophysiology 72, 21342150.
Zhou, Y.X. & Baker, C.L. (1996). Spatial properties of envelope-responsive cells in area 17 and 18 neurons of the cat. Journal of Neurophysiology 75, 10381050
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Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
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