© 2005 Nature Publishing Group http://www.nature.com/natureneuroscience

B R I E F C O M M U N I C AT I O N S

Traveling waves of activity inprimary visual cortex during
binocular rivalry
Sang-Hun Lee1,3, Randolph Blake2 & David J Heeger1
When the two eyes view large, dissimilar patterns that induce
binocular rivalry, alternating waves of visibility are experienced
as one pattern sweeps the other out of conscious awareness.
Here we combine psychophysics with functional magnetic
resonance imaging to show tight linkage between dynamics ofperceptual waves during rivalry and neural events in humanprimary visual cortex (V1).
The cortex is an excitable medium through which waves of neural activity
can propagate1,2. Binocular rivalry, the perceptual alternations induced
when incompatible patterns are presented to the two eyes, provides arare opportunity to observe the perceptual concomitants of neural wave
propagation3. During an alternation, one sees a traveling wave in which
the dominance of one pattern emerges locally and expands progressively
as it renders the other pattern invisible4. Several converging lines of evidence have suggested that primary visual cortex (V1) may be involvedin the spatiotemporal dynamics of these perceptual traveling waves, butthat involvement had not, so far, been demonstrated. Here we use functional magnetic resonance imaging (fMRI) to measure and characterize
traveling waves of cortical activity during binocular rivalry.
Human observers viewed a dichoptic display designed to induce perceptual waves (Fig. 1a). Experiments were carried out with the written
Figure 1 Traveling waves of cortical activity in human V1. (a) Left twopanels, stimuli were rival gratings viewed dichoptically. Right panel(Percept), snapshot of the perceptual traveling wave in which the lowcontrast pattern was seen to spread around the annulus, starting at the top.
(b) Left, anatomical image passing through the posterior occipital lobe,
roughly perpendicular to the calcarine sulcus. Red outline, subregion of V1
corresponding retinotopically to the upper-right quadrant of the stimulus
annulus. Blue outline, subregion of V1 corresponding to the lower-rightquadrant of the stimulus. Middle, time series of the predicted neural activity
according to a simplified model (see Supplementary Methods online). Right,
time series of the measured fMRI responses corresponding to the two outlined
subregions, averaged across ∼1,000 trials for one observer. Red and blue
arrows, times at which corresponding curves peak. (c) Temporal delay in thefMRI responses as a function of cortical distance from the V1 representationof the top of the annulus, categorized by behavioral latency and averaged
across observers. Steeper slope corresponds to slower speed. Larger
y-intercept corresponds to longer initial delay. Error bars, s.e.m. (d) Estimatedpropagation speed of the underlying neural activity, averaged across behavioral
latencies. Dashed line, best fit to the mean across observers.

consent of each observer, and in compliance with the safety guidelines
for MRI research, as approved by the Stanford University Panel on
Human Subjects in Medical Research. The rival images were a lowcontrast radial grating (viewed by one eye) and a high-contrast spiralgrating (viewed by the other eye), each restricted to an annular region of
the visual field centered on the point of fixation. Exploiting the susceptibility of binocular rivalry to transient stimulation5, we triggered shifts
in perceptual dominance through a brief, abrupt increase in contrast
in a small region of the low-contrast grating at the top of the annulus (see Supplementary Methods and Supplementary Fig. 1 online).
This contrast pulse typically evoked a perceptual traveling wave, so thatobservers perceived the local dominance of the low-contrast image as
spreading around the annular region, starting at the top of the annulus
and progressively erasing the high-contrast image from visual awareness4 (Supplementary Video 1 online). Observers pressed a key whena perceptual wave reached a target area (marked by nonius lines) at thebottom of the annulus. This key press triggered the disappearance of thetwo monocular gratings until the beginning of the next trial.

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1Department of Psychology and Center for Neural Science, New York University, 6 Washington Place, 8th floor, New York, New York 10003, USA. 2Department ofPsychology, Vanderbilt University, 512 Wilson Hall, Nashville, Tennessee 37203, USA. 3Present address: Department of Psychology, Seoul National University, Seoul,South Korea. Correspondence should be addressed to D.J.H. (david.heeger@nyu.edu).
Published online 5 December 2004; doi:10.1038/nn1365

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B R I E F C O M M U N I C AT I O N S
If activity in the visual cortex reflects the spatiotemporal dynamics ofrivalry, then there should be a wave of cortical activity coincident withthe perceptual wave (Fig. 1b). Specifically, the peak of the fMRI responses
at locations along the path of the cortical wave should be increasingly
delayed with increasing distance from the cortical representation of the
top of the annulus. This is because (i) locations further from the point oforigin of the traveling wave will respond to the high contrast for longer
durations, and (ii) fMRI responses in V1 increase monotonically withstimulus contrast6. It is important to keep in mind, however, that thephysical contrasts of both rival gratings remained unchanged—only
the perceptual transitions associated with rivalry provided the potentialconditions for traveling waves of cortical activity.
V1 did indeed show traveling waves of activity while observers
experienced perceptual traveling waves (Fig. 1c and SupplementaryVideo 2 online). Gray matter corresponding to the V1 representationof the stimulus annulus was identified using conventional retinotopic
mapping procedures7. For each voxel within this subregion of V1 graymatter, we calculated the temporal delay of the fMRI responses averaged across trials (see Supplementary Methods online). The resulting
temporal delays increased with distance from the V1 representationof the top of the stimulus annulus. The correlation between temporaldelay and cortical distance was statistically significant in each individual
observer (P < 0.05, Pearson χ2 test). This occurred despite the absenceof wave-like changes in the stimulus itself.
The dynamics of these cortical waves of V1 activity correlated withthe latency of the perceptual waves (Fig. 1c). We segregated the trials
into three categories based on the latency of the observers’ key-press
responses and averaged the fMRI data across trials separately for eachof the three ranges of behavioral latencies. Both the speed (slope of theline of best fit) and the initial delay (y-intercept) of the cortical waves
increased with behavioral latency (P < 0.0001, bootstrap statistical test;
see Supplementary Methods online for details).
To compare more directly the fMRI data with the perceptual phenomena during rivalry, we estimated the speed of propagation of
the underlying cortical activity from the measured fMRI responses(Fig. 1d). This was done using a model of the underlying neural activity (Fig. 1b) along with a model for how an fMRI signal depends onunderlying neural activity (see Supplementary Methods online fordetails). In addition to the unknown neural response latencies, themodel had five free parameters: one parameter corresponded to theratio of the amplitudes of the tonic neural activity for each of the twostimulus contrasts, another characterized the amplitude of transientneural responses evoked by abrupt stimulus onset at the beginningof each trial, and three were used to characterize the hemodynamic
impulse response. Values for these five parameters were determined
separately for each observer by fitting the model to the fMRI responses
evoked by physical traveling waves. In a separate ‘replay’ experiment,
sequences of monocular images were shown to observers, mimicking perceptual waves under nonrivalry conditions. We had complete
information about the timing of neural events during this replay
experiment; the neural-response amplitudes and the hemodynamic

NATURE NEUROSCIENCE VOLUME 8 | NUMBER 1 | JANUARY 2005

impulse response were the only parameters that had to be determined,
which was done by fitting the fMRI responses to the physical travelingwaves. With those five parameters fixed, we then fit the model to thefMRI responses measured during rivalry, which resulted in separate
estimates for the latencies of the underlying neural activity for eachvoxel of V1 gray matter. A linear fit of the neural latencies revealed
wave propagation speeds across the three observers of 1.6–2 cm/s;these propagation speeds compare favorably to the speed value of
2.2 cm/s estimated from psychophysical measurements using essentially the same stimulus4.
In summary, the time course of cortical activity varied systematically
across the retinotopic map in V1, in correspondence with the subjective
perception of traveling waves during binocular rivalry. These results
go beyond those from previous single-unit electrophysiology8–10 andneuroimaging11–15 studies by demonstrating that V1 activity reflects thespatiotemporal dynamics of perception during rivalry. Furthermore,
the data show that fMRI is capable of resolving timing differences of∼115 ms over a distance of ∼3.5 mm (Fig. 1c). It remains to be seen
whether these cortical waves originate in V1 via long-range intracorticalconnections or whether they are evoked by feedback from higher-ordervisual cortical areas.
Note: Supplementary information is available on the Nature Neuroscience website.
ACKNOWLEDGMENTS
We thank N. Logothetis, C. Koch and the late F. Crick for comments on an earlier
version of the manuscript. Supported by grants from the National Institutesof Health to D.J.H. (EY12741) and to R.B. (EY14437), and a grant from theKorea Institute of Science & Technology Evaluation and Planning to S.H.L.
(M103KV010021-04K2201-02140). Data were acquired while D.J.H. and S.H.L.
were at Stanford University. Part of this work was completed while R.B. was avisiting scholar at New York University.
COMPETING INTERESTS STATEMENT
The authors declare that they have no competing financial interests.
Received 29 September; accepted 5 October 2004
Published online at http://www.nature.com/natureneuroscience/
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