Processing of first-order motion in marmoset visual cortex
is influenced by second-order motion
NICK BARRACLOUGH,
1
CHRIS TINSLEY,
2
BEN WEBB,
3
CHRIS VINCENT,
4
and ANDREW DERRINGTON
4
1
Department of Psychology, University of Hull, East Yorkshire, United Kingdom
2
Department of Experimental Psychology, University of Bristol, Bristol, United Kingdom
3
School of Psychology, University of Nottingham, Nottingham, United Kingdom
4
The School of Psychology, University of Newcastle, Newcastle, United Kingdom
(Received October 7, 2005; Accepted June 1, 2006!
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%, 67093! of cells ~ V1
73%, 45062; V2 70%, 16023; third visual complex 75%, 608!, 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: Primate, Physiology, V1, Luminance, Contrast
Introduction
We can perceive motion as a result of either the movement of
luminance-defined spatial structures in a visual stimulus, or the
movement of higher-order spatial structures, for example contrast
envelopes or texture borders, ~ Badcock & Derrington, 1985; Der-
rington & Badcock, 1985; Chubb & Sperling, 1988!. The two
types of motion are called, respectively, first-order motion and
second-order motion, ~Cavanagh & Mather, 1989!. First-order
motion information abounds in our moving natural environment,
often accompanied by second-order motion information. Second-
order motion information can be used to break camouflage and
evaluate movement when first-order motion information is unreli-
able or even absent.
There is substantial disagreement in the scientific literature
whether first-order motion and second-order motion are processed
separately. Motion is processed at multiple and distinct stages
within the visual system ~ Zeki, 1990; Movshon & Newsome,
1996! and this have additionally confused the issue. In this study
we address the question of whether first-order motion processing
in V1, V2, and the third visual complex is influenced by an
additional second-order motion signal.
Derrington and Badcock ~1985! found that the discrimination
of the direction of motion of first-order and second-order stimuli
were different. Sensitivity to a moving second-order stimulus was
lower and the necessary temporal resolution of the second-order
stimulus was also lower than that for a moving first-order stimulus.
The authors also found that second-order motion stimuli do not
elicit a motion after-effect and proposed that the human visual
system uses different mechanisms to process first- and second-
order motion ~ Badcock & Derrington, 1985; Derrington & Bad-
cock, 1985!. Many other psychophysical studies have been used to
argue that processing systems for first-order motion and second-
order motion are largely independent ~ Harris & Smith, 1992;
Mather & West, 1993; Ledgeway & Smith, 1994; Lu & Sperling,
1995; Nishida et al., 1997; Scott-Samuel & Georgeson, 1999!.
Separate processing of first-order motion and second-order motion
has also received some support from physiological ~ Zhou & Baker,
1993, 1994; Mareschal & Baker, 1998a! and neurological studies
~ Vaina & Cowey, 1996; Greenlee & Smith, 1997!.
Address correspondence and reprint requests to: Nick Barraclough,
University of Hull, Department of Psychology, East Yorkshire HU6 7RX,
United Kingdom. E-mail: n.barraclough@hull.ac.uk
Visual Neuroscience ~2006!, 23, 815–824. Printed in the USA.
Copyright © 2006 Cambridge University Press 0952-5238006 $16.00
DOI: 10.10170S0952523806230141
815