BINOCULAR RIVALRY AND NEURAL DYNAMICS.

Abstract

The Gestalt psychologists were fascinated with dynamics evident in visual perception, and they theorized that these dynamics were attributable to ever-changing electrical potentials within topographically organized brain fields. Dynamic field theory, as it was called, was subsequently discredited on grounds that the brain does not comprise a unitary electrical field but, instead, a richly interconnected network of discrete computing elements. Still, this modern conceptualization of brain function faces the challenge of explaining the fact that perception is dynamic in space and in time. To pursue the question of visual perception and cortical dynamics, we have focused on spatio-temporal transitions in dominance during binocular rivalry. We have developed techniques for initiating and measuring these transitions psychophysically and for measuring their neural concomitants using functional magnetic resonance imaging (fMRI). Our findings disclose the existence of waves of cortical activity that travel across the retinotopic maps that define primary and secondary visual areas within occipital cortex, in correspondence with the subjective perception of spreading waves of dominance during binocular rivalry. This paper reviews the results from those studies.

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ISSN 1392–0359. PSICHOLOGIJA 2008 38
BINOCULAR RIVALRY AND NEURAL DYNAMICS*
David Heeger
Department of Psychology and Center for
Neural Science
New York University, 6 Washington Place, 8th
floor
New York NY, 10003, USA
E-mail: david.heeger@nyu.edu
Randolph Blake
Centennial Professor of Psychology
Department of Psychology
Vanderbilt University,
Nashville TN 37212, USA
E-mail: randolph.blake@vanderbilt.edu
Sang-Hun Lee
Department of Psychology
Seoul National University,
Gwanak-ro, Gwanak-gu,
Seoul, 151–742, Korea
E-mail: visionsl@snu.ac.kr
The Gestalt psychologists were fascinated with dynamics evident in visual perception, and they theorized
that these dynamics were attributable to ever-changing electrical potentials within topographically
organized brain fields. Dynamic field theory, as it was called, was subsequently discredited on grounds
that the brain does not comprise a unitary electrical field but, instead, a richly interconnected network
of discrete computing elements. Still, this modern conceptualization of brain function faces the
challenge of explaining the fact that perception is dynamic in space and in time. To pursue the question
of visual perception and cortical dynamics, we have focused on spatio-temporal transitions in dominance
during binocular rivalry. We have developed techniques for initiating and measuring these transitions
psychophysically and for measuring their neural concomitants using functional magnetic resonance
imaging (fMRI). Our findings disclose the existence of waves of cortical activity that travel across the
retinotopic maps that define primary and secondary visual areas within occipital cortex, in
correspondence with the subjective perception of spreading waves of dominance during binocular
rivalry. This paper reviews the results from those studies.
Key words: binocular vision, binocular rivalry, visual cortex, fMRI (functional magnetic resonance
imaging), dynamic of neuronal process.
Introduction
Binocular rivalry is the alternation in per-
ception that occurs when the two eyes view
dissimilar monocular patterns (Blake & Lo-
gothetis, 2002). The phenomenon was first
systematically described by C. Wheatstone
(1838) in his landmark monograph on stereop-
sis, and it was subsequently highlighted in the
writings of H. von Helmholtz (1866), William
* The paper was presented at the Symposium “Visual Perception: From Experiments to Modeling” which formed
part of the ICP2008 conference held in Berlin in July 20–25, 2008.
Scientific Editor: Dr. Declan J. McKeefry, Bradford School of Optometry and Vision Sciences, University of
Bradford, UK.

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James (1890) and B. B. Breese (1899). There
now exists a voluminous literature on the
characteristics of binocular rivalry (see reviews
by Walker, 1975; Blake, 2001), and in recent
years significant advances have been made in
identifying the neural concomitants of this
beguiling phenomenon (Leopold &
Logothetis, 1999; Tong et al., 2006).
The purpose of this paper is to summarize
recent work on one particularly intriguing
aspect of binocular rivalry: the transitions
between alternative states of dominance during
which one stimulus emerges from suppression
in a wave-like fashion. The locations in time
and space of these transitions are unpredic-
table, but once started these wave-like
transitions imply the existence of spreading
waves of neural activity. To set the stage for
describing this aspect of rivalry, it is useful to
begin with a summary of two key properties of
binocular rivalry, one having to do with rivalry’s
spatial extent and the other having to do with
its temporal characteristics.
Upon extended viewing of binocular rivalry
between dissimilar monocular targets, it is
readily apparent that the incidence of complete
dominance of one target or the other depends
importantly on the size of those targets
(compare the rivalry associated with the two
pairs of rival stimuli reproduced in Figure 1).
When viewed foveally, rival targets larger than
a degree or so of visual angle can exhibit
significant periods of mixed dominance during
which portions of both targets are simul-
taneously visible within different locations;
these periods of mixed dominance resemble
an ever-changing mosaic comprising bits and
pieces of both eyes’ views. When foveally
viewed, rival targets are relatively small;
however, one tends to experience exclusive
dominance of one target or the other, with
periods of mixed dominance occurring mostly
during transitions from dominance of one to
dominance of the other. This dependence of
exclusive dominance on stimulus size suggests
that rivalry transpires within local zones whose
size is governed by the sizes of the receptive
fields of neurons embodying those zones. In
this regard, it is noteworthy that larger rival
targets imaged within more peripheral regions
of the visual field, away from fixation, are less
susceptible to mixed dominance, implying that
zone sizes scale with retinal eccentricity (Blake
et al., 1992).
Figure 1. Examples of monocular stimuli that, when viewed dichoptically (i. e. separately by the two eyes)
produce binocular rivalry (i. e. fluctuations in perceptual dominance over time). With the smaller pair of
rival stimuli, perceptual dominance tends to correspond to one complete picture or the other, whereas
dominance with the larger pair of rival stimuli is often mixed (i. e. parts of both pictures can be dominant,
yielding a patch-work appearance that changes over time).

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A second key property of binocular rivalry
concerns the pattern of alternations in
dominance over time (see Figure 2). Rather
than switching regularly between one stimulus
and the other, rivalry alternations occur
unpredictably, with the successive durations of
dominance being stochastically independent
(Fox & Hermann, 1967; Lehky, 1988). The
resulting frequency histogram of dominance
durations conforms to the general shape of the
gamma distribution (Levelt, 1965; but see
Brascamp et al., 2005). The average rate of
alternations during rivalry is dependent on
stimulus variables such as luminance (Fox &
Rasche, 1969), contrast (Mueller & Blake,
1989) and spatial frequency (Fahle, 1982).
Observers can lengthen the average duration
of dominance states by intensely focusing
attention on the currently dominant rival
stimulus (Chong et al., 2005), but observers
cannot willfully hold one stimulus dominant
indefinitely: rivalry alternations appear to be
an obligatory outcome of the neural events
underlying rivalry. It is commonly believed that
neural adaptation plays an important role in
promoting rivalry alternations, the idea being
that the strength of the currently dominant
stimulus wanes over time and eventually falls
below some threshold level that tips the
balance of strength in favor of the previously
suppressed stimulus. Pointing to the in-
volvement of adaptation in rivalry alternations
are studies showing that exposure to a pattern
immediately prior to experiencing rivalry
biases initial dominance away from that
stimulus when it is placed in rivalry against
another, unadapted stimulus (e.g., Hancock et
al., 2008). Also, implicating the involvement
of adaptation is a study showing that rivalry
alternations are substantially slowed when rival
targets move smoothly around the visual field,
thereby precluding neural adaptation within
Figure 2. The upper part of the figure shows an example tracking record where an observer presses one
of two keys to indicate which one of two rival stimuli, orthogonally oriented gratings in this example,
is currently dominant. The light- and dark-shaded regions denote dominance of one stimulus or the other.
The histogram in the lower part of the figure shows the frequency distribution for individual perceptual
dominance duration collected over an extended tracking period. Because different observers have different
rates of rivalry alternations, durations are normalized for each observer by dividing individual durations
by that observer’s mean dominance duration.

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any particular region of the retina (Blake et
al., 2003).
These spatio-temporal properties of rivalry
have led to the development of models of rivalry
based on local competition between neural
representations of the competing rival stimuli
(see Figure 3). According to these models,
neurons supporting these competing repre-
sentations exert reciprocal inhibition on one
another, such that the activity associated with one
representation temporarily outstrips the other,
causing dominance of that stronger repre-
sentation in a winner takes all fashion. At the
same time both pools of neurons undergo self-
adaptation, with the strength of adaptation
dependent on the level of activity within those
neurons. The dominant representation, being
temporarily more active, undergoes stronger
adaptation that eventually culminates in a
reversal in the balance of relative activity. This
causes the neural representation of the previously
suppressed stimulus to exceed that of the
previously dominant stimulus, thereby triggering
a switch in the state of rivalry. To instantiate the
irregular durations of dominance during rivalry,
these models typically incorporate internal noise
within some component of the neural circuitry
(Wilson, 2007), and in some neural models this
noise plays a preeminent role (Moreno-Bote et
al., 2007).
This reciprocal inhibition model can differ
in its subtleties (Lehky, 1988; Blake, 1989;
Sugie, 1982; Kalarickal & Marshall, 2000;
Wilson, 2005), but until recently all versions
of the model have been designed to account
for rivalry within a local region of the visual
field, and the transitions between rivalry states
have been treated as all or none phenomena.
Yet we know from simple inspection of rival
stimuli that these transitions are not abrupt and
spatially unitary. When viewing rivalry, people
readily perceive smooth transitions in domi-
nance as one rival stimulus replaces the other
in visual awareness. These orderly transitions
in dominance are particularly conspicuous
when viewing large rival patterns whose
features have global configuration – with these
kinds of stimuli, one perceives waves of
dominance that originate locally and then
spread rapidly over the remainder of the
previously suppressed target. These waves of
dominance are difficult to study, however,
because they arise unpredictably anywhere
within the currently suppressed rival target,
and their directions of spread are typically
unconstrained by the geometry of the rival
targets. Still, the existence of dominance waves
would seem to offer a unique opportunity for
studying cortical dynamics in visual perception,
and for that reason we have sought to develop
Figure 3. A simple neural circuit that uses reciprocal inhibition between two populations of neurons to produce
alternations in activation levels over time. L and R denote left-eye and right-eye stimulation of the two
populations of neurons, denoted here as EL and ER (where E stands for excitatory). The connections labeled “I”
indicate inhibition, and the notations HL and HR denote self-adaptation. With appropriate selection of
parameters, this circuit will exhibit oscillatory activations favoring one neural representation or the other.

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techniques for triggering dominance waves and
controlling their propagation. The following
sections describe the details of our efforts and
the resulting insights gained from studying
dominance waves using brain imaging tech-
niques.
Psychophysical studies of traveling
waves of dominance
Two of us (SHL and RB), in collaboration with
Hugh Wilson, developed a novel procedure for
inducing and measuring dominance waves
(Wilson et al., 2001). Waves were induced with
annular rival targets, essentially one-dimen-
sional shapes that constrained the direction of
motion. The rival targets were circular patterns
like those illustrated in Figure 4, shown here
as a spiral grating presented to one eye and a
radial grating to the other. The observer always
maintained fixation at the center of the circular
patterns, where rivalry was not being induced.
The two monocular rival gratings were
surrounded by identical fusion frames to
promote stable binocular alignment; these
stimuli were displayed on the left and right
halves of calibrated video monitor, and viewed
through a mirror stereoscope. All aspects of
the displays and all trial-related events were
under computer control.
The observer maintained strict central
fixation and depressed and held a designated
key on the computer keyboard when one of
the two rival targets was completely dominant,
with no hint of any portion of the other,
suppressed pattern. The computer then
Figure 4. Stimulus configuration for triggering and measuring traveling waves of dominance. The left-hand
panel shows rival stimuli (high contrast spiral grating and low contrast radial grating) at three different
points in time; note that in the middle part of this sequence, a localized increment in contrast appears in the
upper, left-hand part of the low-contrast, radial grating. This localized pulse will cause that portion of the
radial grating to achieve dominance, and that dominance then spreads to encompass more and more of the
radial grating. The right-hand panel illustrates what typically is experienced by an observer viewing these
rival stimuli.