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

Published online by Cambridge University Press:  04 October 2006

NICK BARRACLOUGH ,
CHRIS TINSLEY ,
BEN WEBB ,
CHRIS VINCENT  and
ANDREW DERRINGTON
NICK BARRACLOUGH
Affiliation:
Department of Psychology, University of Hull, East Yorkshire, United Kingdom
CHRIS TINSLEY
Affiliation:
Department of Experimental Psychology, University of Bristol, Bristol, United Kingdom
BEN WEBB
Affiliation:
School of Psychology, University of Nottingham, Nottingham, United Kingdom
CHRIS VINCENT
Affiliation:
The School of Psychology, University of Newcastle, Newcastle, United Kingdom
ANDREW DERRINGTON
Affiliation:
The School of Psychology, University of Newcastle, Newcastle, United Kingdom
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Abstract

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.

Keywords

PrimatePhysiologyV1LuminanceContrast
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 5 , September 2006 , pp. 815 - 824
Copyright
2006 Cambridge University Press

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References

REFERENCES

Albrecht, D.G. & De Valois, R.L. (1981). Striate cortex responses to periodic patterns with and without the fundamental harmonics. Journal of Physiology 319, 497–514.Google Scholar
Badcock, D.-R. & Derrington, A.-M. (1985). Detecting the displacement of periodic patterns. Vision Research 25, 1253–1258.Google Scholar
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, 169–180.Google Scholar
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, 1132–1145.Google Scholar
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103–129.Google Scholar
Chaudhuri, A. & Albright, T.D. (1997). Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1. Visual Neuroscience 14, 949–962.Google Scholar
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, 1986–2007.Google Scholar
Clifford, C.W.G. & Vaina, L.M. (1999). A computational model of selective deficits in first and second-order motion processing. Vision Research 39, 113–130.Google Scholar
Derrington, A.M. & Badcock, D.R. (1985). Separate detectors for simple and complex grating patterns? Vision Research 25, 1869–1878.Google Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.Google Scholar
Edwards, M. & Nishida, S. (2004). Contrast-reversing global-motion stimuli reveal local interactions between first- and second-order motion signals. Vision Research 44, 1941–1950.Google Scholar
Felisberti, F. & Derrington, A.M. (2001). Long-range interactions in the lateral geniculate nucleus of the New-World monkey, Callithrix jacchus. Visual Neuroscience 18, 209–218.Google Scholar
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, 804–818.Google Scholar
Harris, L.R. & Smith, A.T. (1992). Motion defined by second-order characteristics does not evoke optokinectic nystagmus. Visual Neuroscience 9, 565–570.Google Scholar
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, 297–306.Google Scholar
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, 1771–1783.Google Scholar
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, 254–265.Google Scholar
Ledgeway, T. & Smith, A.T. (1994). Evidence for separate motion-detecting mechanisms for first- and second-order motion in human vision. Vision Research 34, 2727–2740.Google Scholar
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, 27–35.Google Scholar
LeVay, S. & Gilbert, C.D. (1976). Laminar patterns of geniculocortical projection in the cat. Brain Research 113, 1–19.Google Scholar
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, 5–19.Google Scholar
Lu, Z.-L. & Sperling, G. (1995). The functional architecture of human visual motion perception. Vision Research 35, 2697–2722.Google Scholar
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, 249–261.Google Scholar
Mareschal, I. & Baker, C.L. (1998a). A cortical locus for the processing of contrast-defined contours. Nature Neuroscience 1, 150–154.Google Scholar
Mareschal, I. & Baker, C.L. (1998b). Temporal and spatial response to second-order stimuli in cat area 18. Journal of Neurophysiology 80, 2811–2823.Google Scholar
Mather, G. & West, S. (1993). Evidence for second-order motion detectors. Vision Research 33, 1109–1112.Google Scholar
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrode. Medical and Biological Engineering 10, 495–504.Google Scholar
Movshon, J.A. & Newsome, W.T. (1996). Visual response properties of striate cortical neurons projecting to area MT in macaque. Journal of Neuroscience 16, 7733–7741.Google Scholar
Nishida, S., Ledgeway, T., & Edwards, M. (1997). Dual multiple-scale processing for motion in the human visual system. Vision Research 37, 2685–2698.Google Scholar
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, 3242–3254.Google Scholar
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, 459–462.Google Scholar
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, 547–567.Google Scholar
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, 327–339.Google Scholar
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, 164–191.Google Scholar
Scott-Samuel, N.E. & Georgeson, M.A. (1999). Does early non-linearity account for second-order motion? Vision Research 39, 2853–2865.Google Scholar
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, 158–167.Google Scholar
Taub, E., Victor, J.D., & Conte, M.M. (1997). Nonlinear preprocessing in short-range motion. Vision Research 37, 1459–1477.Google Scholar
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, 1225–1232.Google Scholar
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, 1–10.Google Scholar
Wilson, H.R., Ferrera, V.P., & Yo, C. (1992). A psychophysical motivated model for two-dimensional motion perception. Visual Neuroscience 9, 79–97.Google Scholar
Zeki, S. (1990). The motion pathways of the visual cortex. In Vision: Coding and efficiency, ed. Blakemore, C., pp. 321–345. 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, 98–101.Google Scholar
Zhou, Y.X. & Baker, C.L. (1994). Envelope-responsive neurons in areas 17 and 18 of cat. Journal of Neurophysiology 72, 2134–2150.Google Scholar
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, 1038–1050Google Scholar