Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception.

Abstract

Consciousness has been proposed to emerge from functionally integrated large-scale ensembles of gamma-synchronous neural populations that form and dissolve at a frequency in the theta band. We propose that discrete moments of perceptual experience are implemented by transient gamma-band synchronization of relevant cortical regions, and that disintegration and reintegration of these assemblies is time-locked to ongoing theta oscillations. In support of this hypothesis we provide evidence that (1) perceptual switching during binocular rivalry is time-locked to gamma-band synchronizations which recur at a theta rate, indicating that the onset of new conscious percepts coincides with the emergence of a new gamma-synchronous assembly that is locked to an ongoing theta rhythm; (2) localization of the generators of these gamma rhythms reveals recurrent prefrontal and parietal sources; (3) theta modulation of gamma-band synchronization is observed between and within the activated brain regions. These results suggest that ongoing theta-modulated-gamma mechanisms periodically reintegrate a large-scale prefrontal-parietal network critical for perceptual experience. Moreover, activation and network inclusion of inferior temporal cortex and motor cortex uniquely occurs on the cycle immediately preceding responses signaling perceptual switching. This suggests that the essential prefrontal-parietal oscillatory network is expanded to include additional cortical regions relevant to tasks and perceptions furnishing consciousness at that moment, in this case image processing and response initiation, and that these activations occur within a time frame consistent with the notion that conscious processes directly affect behaviour.

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Rhythms of Consciousness: Binocular Rivalry Reveals
Large-Scale Oscillatory Network Dynamics Mediating
Visual Perception
Sam M. Doesburg1*, Jessica J. Green2, John J. McDonald2, Lawrence M. Ward1,3
1Psychophysics and Cognitive Neuroscience Laboratory, Department of Psychology, University of British Columbia, Vancouver, British Columbia, Canada, 2Department
of Psychology, Simon Fraser University, Burnaby, British Columbia, Canada, 3Brain Research Centre, University of British Columbia, Vancouver, British Columbia, Canada
Abstract
Consciousness has been proposed to emerge from functionally integrated large-scale ensembles of gamma-synchronous
neural populations that form and dissolve at a frequency in the theta band. We propose that discrete moments of
perceptual experience are implemented by transient gamma-band synchronization of relevant cortical regions, and that
disintegration and reintegration of these assemblies is time-locked to ongoing theta oscillations. In support of this
hypothesis we provide evidence that (1) perceptual switching during binocular rivalry is time-locked to gamma-band
synchronizations which recur at a theta rate, indicating that the onset of new conscious percepts coincides with the
emergence of a new gamma-synchronous assembly that is locked to an ongoing theta rhythm; (2) localization of the
generators of these gamma rhythms reveals recurrent prefrontal and parietal sources; (3) theta modulation of gamma-band
synchronization is observed between and within the activated brain regions. These results suggest that ongoing theta-
modulated-gamma mechanisms periodically reintegrate a large-scale prefrontal-parietal network critical for perceptual
experience. Moreover, activation and network inclusion of inferior temporal cortex and motor cortex uniquely occurs on the
cycle immediately preceding responses signaling perceptual switching. This suggests that the essential prefrontal-parietal
oscillatory network is expanded to include additional cortical regions relevant to tasks and perceptions furnishing
consciousness at that moment, in this case image processing and response initiation, and that these activations occur
within a time frame consistent with the notion that conscious processes directly affect behaviour.
Citation: Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009) Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics
Mediating Visual Perception. PLoS ONE 4(7): e6142. doi:10.1371/journal.pone.0006142
Editor: Teresa Serrano-Gotarredona, National Microelectronics Center, Spain
Received September 19, 2008; Accepted June 17, 2009; Published July 3, 2009
Copyright: ? 2009 Doesburg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This project was supported by an NSERC operating grant investigating the relationship between synchronous neural oscillations and cognitive
processing. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: sdoesburg@cw.bc.ca
Introduction
Consciousness has been envisioned as a dynamic global
workspace wherein unified experience is assembled out of relevant
constituent elements [1,2]. This view is consistent with the notion
that consciousness is chiefly characterized by the qualities of
dynamism, selectivity, and integrated subjective experience,
attributes explained by the postulation that experience is
equivalent to informational integration of relevant neural elements
into a large-scale complex [3]. In such a view, the contents of
experience would be defined by the activity of the largest and most
dominant coalition of functionally integrated neurons at a given
moment [3,4]. Any such process would necessitate continuous and
complex rearrangement of neural populations across widespread
and diverse cortical regions, a feat that has been attributed to
oscillatory dynamics [e.g. 5]. Low gamma-band (30 Hz to 50 Hz)
synchronization between neural groups coding the various features
of objects currently populating experience has been proposed as a
mechanism for such dynamic functional integration in the brain,
and has been suggested to be the biological basis of perceptual
experience and feature binding [6–8]. It has been proposed that
synchronization enables transient functional integration between
specific neural groups as bursts of action potentials are consistently
exchanged during the depolarized phase of the receiving neurons’
ongoing membrane potential fluctuations, thereby enhancing
communication between populations oscillating in synchrony [9].
Support for this notion can be drawn from findings that mutual
influence between neural populations is positively correlated with
gamma-band synchronization in both intra-regional and large-
scale oscillatory dynamics [10,11].
Empirical evidence for the involvement of gamma-band neural
synchronization in perceptual binding and awareness flows from
diverse lines of research. Gamma-band synchronization in
primary visual cortex of cats, for example, occurs most strongly
between columns responding to a common object, presumably
implementing feature binding and figure-ground segregation [12–
14]. Stimulus dependent synchronization in the gamma frequency
range has also been recorded between cortical areas [15–17].
Local and long-range gamma-band electroencephalographic
(EEG) phase synchronization have been shown to index the onset
of coherent visual perception [18,19]. The integration of local
features in one visual hemifield into a global percept involving
both hemifields, as well as the perception of apparent motion
across visual hemifields, is accompanied by interhemispheric
gamma-band EEG phase coupling [20,21]. Results such as these
have led to the postulation that the emergence of organized
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perception corresponds to the reordering of a large-scale
representational ensemble by way of oscillatory synchronization
in the gamma frequency range [22]. We propose that this
mechanism can account for the selective integration of contents
into a large-scale neural coalition determining the momentary
furnishings of experience. The parameters governing cortical
oscillations are also dynamic, allowing for the integration,
disintegration, and reconstruction of gamma-oscillatory assemblies
in time. Accordingly, we propose that large-scale gamma-band
synchronization constitutes an oscillatory substrate for the stream
of consciousness.
Evidence for this proposed essential relationship between
gamma oscillations and consciousness is not limited to feature
binding. Large-scale gamma EEG synchronization is greater when
a masked stimulus is consciously perceived than when it is not
[23]. Similarly, rapid serial visual presentation has been used to
demonstrate that conscious perception of a stimulus is associated
with greater inter-regional gamma-band phase synchronization,
relative to stimuli that are not perceived [24]. The onset of a new
visual percept, gauged by perceptual switching in binocular
rivalry, coincides with a transient increase in inter-regional
gamma-band phase synchronization [25]. Cognitive processes
closely associated with consciousness, namely attention and
working memory, have also been robustly associated with the
synchronization of gamma rhythms [see 26 for review]. Previous
research has also revealed that coherent thalamo-cortical and
cortico-cortical gamma rhythms are associated with mammalian
consciousness, as they are characteristic of CNS states associated
with experience (wakefulness and REM sleep). Such rhythms also
have been proposed to be the neurobiological basis for
consciousness, a view supported by the observation that functional
decoupling of thalamus and cortex is a cardinal property of
general anesthesia [8,27–30].
If gamma rhythms embody an essential feature of the biological
basis of consciousness, and if gamma-band synchronization of
selective neural populations constructs a large-scale complex
defining the contents of consciousness, as we have proposed, then
some mechanism must exist to govern the evolution of such a
network over time in order to account for the dynamism of
experience. Notably, modulation of intra-regional gamma-band
(80–150 Hz) synchronization at a frequency in the theta band (4–
7 Hz) has been observed using subdural electrodes on human
cortex, with gamma envelope amplitude being most pronounced
during the trough of the theta cycle [31]. Moreover, this
relationship is accentuated during active cognitive processing,
particularly within task-relevant cortical regions [31]. This
important result suggests that the construction and degradation
of low gamma-band (30–50 Hz) oscillatory neural ensembles
might also be governed by theta rhythms. Locking of low gamma-
band synchronization to theta oscillations has been associated with
an array of cognitive processes including working memory,
attention, and perceptual organization [19,25,32–34]. Transient
and periodic desynchronization of gamma rhythms, or phase
scattering, has also been observed between periods of synchroni-
zation [i.e. 19]. Similarly, periods of recurrent increased long-
range gamma-band phase locking consistent with a theta-
frequency modulation are often interposed with periods of baseline
level phase locking [25,35]. We interpret such results as indications
that theta-modulated gamma synchronization serves to organize
transient functional networks across time. Specifically, we propose
that large-scale ensembles synchronously oscillating in the low
gamma frequency range enable transient functional integration of
task- and/or percept-specific neural populations, and that theta
rhythms govern the temporal dynamics according to which the life
cycle of individual gamma-oscillatory ensembles are organized.
This interpretation also suggests that only one truly discrete
perceptual experience may exist within a single theta cycle, and
that the emergence of new perceptual experiences may be time
locked to a particular phase of ongoing cortical theta rhythms.
Ascertaining the neural correlates of perceptual consciousness
requires separation of brain processes related to experience from
those embodying non-conscious stimulus processing, a distinction
made possible using binocular rivalry [36]. Binocular rivalry has
been employed to study the relationship between neural oscillations
and consciousness using flickering, frequency-tagged stimuli to
identify neural populations responding to rivaling images. Such
studies revealed that when a frequency-tagged image is perceived,
increasedlocalandlong-rangeneuralsynchronizationisobservedat
the flicker frequency of the stimulus, reinforcing the view that
consciousnessisassociated with large-scale synchronouslyoscillating
neural ensembles [37,38]. Localization of magnetoencephalo-
graphic rhythms generated in this fashionreveals widely distributed,
localized sources of flicker-entrained neural activity in the cortex
[39]. Importantly, when the flickering stimulus is dominant in the
rivalry, and is thus perceived consciously, inter-regional phase
synchronization between the locally synchronous sources at the
tagged frequency is also at its peak, and decreases sharply when the
flickering stimulus becomes suppressed and disappears from
consciousness. This incisive study indicates that the emergence of
a new visual percept relates to the synchronization of rhythms
within distributed cortical regions and the formation of a large-scale
oscillatory network by means of inter-regional synchronization,
consistent with the notion that visual consciousness is embodied by
large-scale coalitions of neurons wherein the contents of perception
correspond to what is represented by the victor among competing
ensembles [4]. This is the current horizon of our understanding.
Unfortunately, because these seminal studies focused on exogenously
induced rhythms, this understanding leaves undetermined which
endogenous rhythms might govern dynamic cortical networks relevant
to conscious perception.
We propose that the contents of consciousness are defined by
which neural populations are integrated into a large-scale gamma-
synchronous ensemble at any given time. We further propose that
the formation and dissolution of these functional assemblies occurs
at a frequency in the theta band, which effectively places temporal
constraints on the emergence of new, discrete, perceptual
experiences. Two previous key results support this view: (1) When
a stimulus is perceived, a second stimulus occurring approximately
180 ms to 500 ms afterwards often fails to reach consciousness
[40]. This time range corresponds to oscillation frequencies from
about 5.5 Hz to 2 Hz, overlapping the lower part of the classical
theta band (4–7 Hz). Moreover, performance on the second
stimulus is worst in most experiments at an interstimulus interval
of about 225 ms, which corresponds to about 4.4 Hz, a low-theta
frequency. We interpret such results as indications that one can
have only one discrete experience every theta cycle, effectively
implementing a ‘speed limit’ on conscious perception. This
phenomenon, dubbed the ‘‘attentional blink’’ has previously been
proposed to originate at least partly from the suppression of
gamma rhythms, and it has been demonstrated that increased
inter-regional gamma-band EEG phase synchronization is associ-
ated with successful target detection under these rapid serial visual
presentation conditions [24,41]. (2) In a previous study we
demonstrated that the onset of a new percept in binocular rivalry
coincides with a burst of large-scale gamma-band phase
synchronization which was situated within a procession of
gamma-band synchronizations that periodically recurred at a
theta rate [25]. These previous findings have led us to the
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hypothesis that the onset of new visual percepts may be
implemented by a recurrent gamma-oscillatory network that is
phase-locked to an ongoing cortical theta rhythm.
In order to test the hypothesis that large-scale gamma-
oscillatory neural assemblies of relevant cortical regions are
synchronized and desynchronized according to a theta cycle that
also determines the timing of new perceptual experiences, we
recorded EEG data while subjects viewed rivaling visual images
and pressed buttons to indicate which stimulus was being
perceived at any given moment. Data epochs time-locked to
button presses indicating perceptual switching were extracted from
the continuous recording. The resulting time series of scalp
voltages were then transformed into the frequency domain to
reveal periodic gamma activations that recur at a theta rate
preceding the button presses indicating the onset of new percepts.
Beamformer analysis was employed to reveal the cortical
generators of transient and periodic gamma-band activations
(local synchronizations) locked to a theta cycle by comparing these
periods to the interposed period of relative inactivity (local
desynchronization) between them (Figure 1). A dipolar source
montage was seeded according to foci of cortical gamma-band
activations identified by beamformer and filtered time series from
these sources were assessed for cross-frequency coupling between
theta phase and gamma amplitude. Inter-regional gamma-band
phase synchronization was also assessed between cortical gener-
ators of gamma rhythms during these periods of activity, as was
cross-frequency coupling between theta phase in the relevant
generators of a pair and gamma-band phase synchronization
between them. These analyses directly test the hypothesis that
theta-modulated gamma-band synchronization within a network
of relevant cortical regions represents the periodic formation of
transient functional ensembles relevant to perceptual experience.
Results
Binocular rivalry induced stable patterns of perceptual domi-
nance with a mean duration of 782 ms and a standard deviation of
737 ms (Figure 2). The frequency distribution of dominance
periods was well-fitted by a gamma distribution in line with
previous binocular rivalry results [42], although the highly
significant chi-squared value indicates that there are some
departures.
Periodic gamma-band activation time-locked to
perceptual switching
Transformation of EEG scalp activity into the frequency
domain, performed using the Brain Electrical Source Analysis
software suite (BESA 5.2; Megis Software), revealed transient and
periodic gamma activations preceding button presses indicating
the onset of a new percept. These transient increases in local
gamma synchronization displayed a frontocentral scalp distribu-
tion (Figure 3a) and recurred at a rate consistent with a theta cycle,
as well as displaying a trough at about 400 ms prior to button
presses (Figure 3b).
Beamformer analysis was employed to image the neural
generators of gamma-band activation occurring 220–280 ms and
540–600 ms prior to responses, relative to a window of equivalent
length in the intervening period from 370–430 ms prior to
responses (see Figure 3b). This baseline period interposed between
two windows of interest was chosen because gamma-band phase-
scattering, which occurs between periods of gamma synchroniza-
tion, is understood to be a period wherein transient oscillatory
networks are dissolved (see discussion). Accordingly, this analysis
aimed to image a recurrently activated coalition of cortical regions
relative to a period during which this network would be
Figure 1. a,b) The left and right eye stimuli, respectively. c) Schematic representation of the stream of perceptual consciousness wherein discrete
moments of perceptual experience coincide with gamma-band synchronization, itself locked to a theta cycle. Periodic gamma-band synchronization
is locked to the onset of new conscious percepts and hence to button presses signaling perceptual switching. We imaged these oscillatory cortical
networks by comparing gamma synchronization during periodic activations to the intervening period of relative desynchronization. In this figure
0 ms indicates button presses indicating the onset of a new percept. The preceding 2600 to 2540 ms and 2280 to 220 ms analysis windows, as well
as the 2430 to 2370 ms baseline interval, are depicted.
doi:10.1371/journal.pone.0006142.g001
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desynchronized (see Figure 1), i.e. during the trough in gamma
spectral power at around 400 ms prior to a response. The 2220 to
2280 ms and 2540 to 2600 ms intervals were chosen because (i)
these were distinct peaks in the recurrent gamma activation
relative to the intervening baseline period, (ii) they are consistent
with earlier results pertaining to gamma-band neural synchroni-
zation time-locked to perceptual switching in binocular rivalry
obtained using a similar paradigm [25], and (iii) the 2220 to
2280 ms period corresponds to reaction times expected in a
simple perceptual task, suggesting that perceptual switching during
this period may have initiated behavioural responses.
Beamformer analysis imposes a spatial filter to identify
activation within a specified time-frequency window. For each
voxel, an activation value is assigned by removing correlations
with all other voxels. A frequency window of 35 Hz to 45 Hz was
chosen for beamformer source analysis as this bandwidth has been
most reliably associated with both intra-regional and inter-regional
gamma-band synchronization relevant to conscious experience,
feature binding, the dynamics of perceptual organization, and
specifically perceptual switching in binocular rivalry [12–21,25–
28].
Distributed gamma-oscillatory networks time-locked to
perceptual switching
Beamformer imaging of gamma-band activation revealed
multiple generators in both 220–280 ms and 540–600 ms pre-
response windows. In the 540–600 ms pre-response interval,
activation reached the 0.05 level of statistical significance in right
precuneus(PreC),bilateral
(DLPFC), bilateral superior frontal gyrus (SFG) and right
precentral gyrus (PreCG); in the 2220 to 2280 ms interval all
aforementioned sources were significantly activated as well as left
precentral gyrus and right inferior temporal gyrus (ITG) (Table 1;
Figure 4). Importantly, prefrontal and parietal areas were active in
both 220–280 ms and 540–600 ms time windows. These areas are
thought to be of particular relevance to conscious experience (see
dorsolateral prefrontalcortex
[43] for review). Right inferior temporal cortex (ITG) and left
motor cortex (PreCG) displayed significant activation only in the
220–280 ms time window. As all subjects responded using only
their right hand, the left motor cortex was directly responsible for
initiating button presses. The rivaling stimuli in this experiment
were images consisting of complex patterns (see Figure 1),
significant in this context because the right inferior temporal
cortex is known to be particularly relevant for the processing of
this type of stimulus [44], including during rivalry of complex
Figure 2. Distribution of durations for perceptual dominance
periods. Data shown here were obtained from the 9 subjects included
in the EEG analyses. Black curve indicates prediction of a gamma
distribution with scale parameter=400, shape parameter=2.1, fitted to
durations,4001 ms. Although the chi-squared value is highly signifi-
cant the distribution fits well. It deviates most markedly for the shortest
durations (of which there are more than predicted) and durations from
about 1200 ms to 2000 ms (of which there are fewer than predicted).
doi:10.1371/journal.pone.0006142.g002
Figure 3. a) Topography of 35–45 Hz scalp spectral power during the
2540 to 2600 ms and 2220 to 2280 ms intervals, relative to the
baseline interval, for the (R) right side, (L) left side and (T) top view. b)
Periodic bursts of gamma-band scalp activity time-locked to button
presses (at 0 ms) indicating perceptual switching. Depicted is gamma-
band power averaged across subjects and across the 30 electrodes
where gamma activity was most clearly expressed (see Methods). Solid
lines denote time-frequency windows used for beamformer source
localization; dotted lines denote the baseline.
doi:10.1371/journal.pone.0006142.g003
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patterns [45]. Activation of right motor cortex was observed
during both 220–280 ms and 540–600 ms time windows.
Inter-regional gamma-band phase synchronization
We hypothesized that gamma-band phase synchronization
would be observed between cortical areas displaying increased
gamma-band activation during the 220–280 ms and 540–600 ms
pre-response windows. In our view, gamma synchronizations
recurring at a theta rate represent the integration of relevant
neural populations into large-scale ensembles. This entails
functional integration across regions by means of gamma-band
phase synchronization. Again, this synchronization would be
expected relative to phase scattering of gamma rhythms in the
period intervening between the 220–280 ms and 540–600 ms pre-
response windows. To assess gamma-band phase synchronization
between neural sources we extracted epoched time-series data
from all sources identified by the beamformer analysis in the 2220
to 2280 ms and 2540 to 2600 ms time windows using a source
montage (BESA 5.2; Megis Software). Phase locking values (PLVs)
were then computed to assess inter-regional synchronization
relative to the 370–430 ms baseline period. This analysis revealed
gamma-band phase synchronization between many pairs of
activated cortical regions in both the 220–280 ms and 540–
600 ms time windows, and particularly in the 220–280 ms window
related to the onset of a new percept (Figure 4). Moreover, the
observed inter-regional gamma-band synchronizations appear to
partake of an ongoing pattern of intra-regional synchronizations
that recur at a frequency in the theta band. This is evidenced by
the ordered procession of increases in inter-regional gamma-band
synchronization in advance of button presses, which is accompa-
nied by largely coincident increases in intra-regional gamma-band
neuronal synchronization (Figure 5). The ongoing rhythm of both
intra-regional and inter-regional gamma-band synchronization is
consistent with a theta rate of roughly 4–6 Hz (see Figure 5).
Modulation of gamma-band network activity by theta
phase
The above results suggest that the activation of a gamma-
oscillatory network of cortical areas is modulated by the phase of
theta-band oscillations within those brain regions. To test this
hypothesis directly we examined whether gamma (40 Hz, actually
38–42 Hz filtered) z) Hamplitude was modulated by theta (6 Hz,
actually 5.7–7.3 Hz filtered) phase in each of the cortical regions
identified by beamformer analysis. In this analysis we took the
theta phases and gamma amplitudes directly from the analytic
signal over entire 1000 ms pre-response epochs and did not
normalize them relative to the 370–430 ms baseline (see Methods).
That baseline period, rather, was included in each epoch. This
means that 6 theta cycles occurred in each epoch, although
probably not exactly the same 6 cycles. Statistically significant
(p,0.05, two-tailed) modulation of gamma amplitude by theta
phase was found in bilateral SFG, left DLPFC, and right PreC
(Figure 6). Modulation of gamma amplitude by theta phase was
also apparent in right DLPFC and right ITG, but failed to reach
statistical significance for at least two successive bins (see methods).
We thus identified significant modulation of gamma activity by
theta phase in four of the five areas involved in the recurrent
gamma-oscillatory network time-locked to perceptual switching.
Interestingly, the relationship of gamma amplitude to theta phase
was virtually identical for the two SFG sites, and also for left
DLPFC, right PreC and right ITG, but differed between these two
groups by approximately p radians (180u). Moreover, neither of
the peaks of gamma amplitude occurred at the theta trough, as
found by Canolty et al [31] for 80–150 Hz amplitude, but rather
peaks in both sub-groups occurred nearer to the zero-crossing of
the theta oscillation about p/4 radians from the theta minimum
(which would occur around6p).
Phase synchronization of gamma-band oscillations between
cortical regions was also found to be modulated by theta phase.
Table 2 and Figure 7 display the results of this analysis for all pairs
that were active in both the 220–280 ms and 540–600 ms time
windows. Again, in this analysis we used the same 1000 ms pre-
response epochs and theta phases and gamma phase locking values
were not normalized relative to the 370–430 ms baseline; rather
their values in that baseline period were included in the analysis.
As can be seen from Table 2, gamma-band phase synchronization
was modulated by the phase of theta oscillations in at least one of
the two regions involved for many of the region pairs. Importantly,
synchronization of parietal and frontal areas was modulated either
by parietal or frontal theta phase, or both, for all but the right
superior frontal gyrus. Moreover, there was also significant
Figure 4. Surface projected regional gamma-band activations,
and inter-regional gamma-band synchronization in the 540–
600 ms and 220–280 ms pre-response intervals. For clarity,
separate images are provided for (R) right intrahemispheric, (L) left
intrahemispheric and (I) interhemispheric synchronization across
cortical regions. Lower brain figures show surface projected anatomical
loci for all identified gamma-band activations.
doi:10.1371/journal.pone.0006142.g004
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modulation of phase locking among frontal areas by theta phase in
one or both areas of a pair. Modulation of gamma-band phase
locking by theta phase was also found between R PreCG and PreC
and between R PreCG and frontal sources. These modulations
involving R PreCG were, however, generally less pronounced that
synchronization between prefrontal and parietal regions. As was
found in the case of the amplitude modulations, these phase
synchronization modulations did not always coincide with either a
peak or a trough in the theta rhythm. They are evidence, however,
Figure 5. a) Time-course of averaged gamma-band phase synchroni-
zation (standardized PLV) between cortical regions identified by
beamformer source localization preceding the onset of stable percepts.
b) Time-course of averaged intra-regional neural synchronization
preceding the onset of stable percepts (standardized amplitude from
the analytic signal analysis) at centre frequency identified for inter-
regional synchronization (33 Hz).
doi:10.1371/journal.pone.0006142.g005
Figure 6. Theta-modulation of gamma amplitude. Dotted lines
represent the 97.5 (top) and 2.5th(bottom) percentiles and the dark
black line indicates the mean of the surrogate distribution for each of
the 60 bins of the theta cycle. Jagged red line denotes the mean non-
normalized gamma amplitude in each bin. When the gamma amplitude
was greater than or less than the surrogate line for two or more
successive bins we considered the departure to be significant (p,0.05,
two tailed). Left PreCG and right PreCG plots are not shown; they
resemble the plot for right DLPFC and show no significant relationship
between theta phase and gamma amplitude. Radians on the x-axis are
in reference to a cosine wave, which is maximal at 0 radians; one cycle
of a 6 Hz cosine wave (thin black line) is superimposed on the graph.
doi:10.1371/journal.pone.0006142.g006
Table 1. Statistical significance level for gamma-band sources in identified periods of scalp gamma activity and locations of peak
activation used to seed the dipole source montage.
SourceBrodmann Area
MNI Coordinates (mm)
540–600 ms 220–280 ms
xyz
R PreC7 22
268 52p,0.05p,0.01
L DLPFC8
224 3051p,0.05*
p,0.01
R DLPFC8 3434 41p,0.05*
p,0.05
L SFG 10
217 668p,0.01p,0.01*
R SFG 10 19668p,0.01p,0.01
L PreCG6
258
25 37 n.s.p,0.01
R PreCG6 49
25 36p,0.01p,0.01
R ITG 2061
227
223n.s.p,0.05
Abbreviations: R, right; L, left; PreC, precuneus; DLPFC, dorsolateral prefrontal cortex; SFG, superior frontal gyrus; PreCG, precentral gyrus; ITG, inferior temporal
gyrus; n.s., not significant.
*indicates instances where the 3D rendered activation was ambiguous and confirmatory statistics were performed on peak voxels.
doi:10.1371/journal.pone.0006142.t001
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of a strong association between inter-regional gamma-band
synchronization and the phases of ongoing theta-band cortical
rhythms.
Thebeamformer and phase lockinganalysesuncovered a gamma
oscillatory network which is recurrently activated and integrated at
a theta rate. Activation and inter-regional synchronization in this
network is modulated by theta phase but, paradoxically, the precise
relationship to theta oscillations differs between sources and source
pairs. This suggests that theta rhythms differ in phase across the
activated regions. To investigate this we analyzed theta phase
relationships between activated cortical areas. Figure 8 and Table 2
display the results of analysis of these data for the relationship
between non-normalized theta phases in the various region pairs.
Clearly there is a strong relationship for all of them, akin to
significant phase locking, but the various rhythms clearly do not
correspond to a single, trans-cortical rhythm. Rather, there is a
tendency for the theta rhythms in the various brain areas to be
phase locked with varying amounts of phase difference. This makes
it possible for gamma rhythms locked locally to theta phase in their
own region to also be locked across regions, and to follow the theta
rhythms in inducing perceptual changes.
Discussion
Large-scale oscillatory networks and perceptual
consciousness
We have demonstrated that button presses indicating the onset
of a new percept in binocular rivalry of complex patterns are
preceded by time-locked bursts of gamma-band activation that
recur at a theta rate. Source imaging of gamma-band activations
220–280 ms and 540–600 ms prior to responses revealed a
recurrent network of prefrontal and parietal areas consistent with
numerous fMRI investigations implicating these regions in
perceptual transitions in binocular rivalry and in alternations of
bistable figures [see 43,46 for reviews]. Critically, this prefrontal-
parietal network has been shown to be engaged when changes in a
visual scene are detected, confirming that it is relevant to the
updating of perceptual consciousness in general and not only to
bistable perception [47]. The similarity of our source solution to
cortical networks identified by hemodynamic neuroimaging also
indicates that observed gamma-band activations are unlikely to
arise from ocular artifacts such as microsaccades, which would be
localized to the eyes and rejected from our solution. We also
demonstrated that the cortical sources of gamma activity in the
220–280 ms and 540–600 ms pre-response time windows display
increases in inter-regional gamma-band phase synchronization,
thereby integrating those regions into a transient functional
network. This result supports the view that consciousness emerges
as a product of large-scale brain integration implemented by
synchronization of relevant neural populations in the gamma-
band [6,7]. We interpret this as reflecting the selective integration
of information represented in relevant cortical regions into a large-
scale assembly that constitutes a global workspace for conscious-
ness [1,3]. Periodic activation of, and integration within, this
network would thus correspond to the formation of a new large-
scale assembly defining conscious contents and, in the context of
the present inquiry, a window of time during which the onset of a
new percept occurs.
In this view, prefrontal cortex is an essential component of the
‘consciousness network’ because of its relevance for integration
generally and for self-awareness, whereas parietal cortex is critical
as it contains a multimodal representation of space in which the
representation of self is located relative to the perceptual world
[43,48,49]. The precuneus, identified in the present study, is also
specifically associated with the experience of agency, mental
imagery, episodic memory retrieval, and first person perspective
taking, and has abundant connections with prefrontal cortex,
further implicating it in perceptual experience [see 48 for review].
The spread of surface-rendered activation on the cortical surface
suggests that parietal activity may have also extended to other
regions relevant for perceptual space. The integrated intersection
of ‘observing’ and ‘representing’ faculties situated in prefrontal and
parietal cortex, respectively, may thus reflect the substrate of
perceptual consciousness [4,50].
Interestingly, primary visual cortex was not identified as a
generator of gamma rhythms time-locked to perceptual switching.
Although required for perceptual experience, neuroanatomical
and psychophysical data suggest that we do not directly experience
activity in striate cortex [43,51]. This supports the view that the
large-scale oscillatory network detailed here is essentially related to
perceptual experience itself, and not to those unconscious
functions that give rise to changes within it. It is known that
perceptual transitions in binocular rivalry involve primary visual
cortex [see 52 for review], and are associated with changes in
gamma-band synchronization within primary visual cortex
[53,54]. It is a matter of some debate, however, whether activity
Figure 7. Theta-modulation of gamma-band inter-regional
phase locking. Dotted lines represent the 97.5 (top) and 2.5th
(bottom) percentiles and the dark black line indicates the mean of the
surrogate distribution for each of the 60 bins of the theta cycle. Jagged
red line denotes the non-normalized gamma-band phase locking value
in each bin. When phase-locking was greater than or less than the
surrogate line for two or more successive bins we considered the
departure to be significant (p,0.05, two-tailed). Radians on the x-axis
are in reference to a cosine wave, which is maximal at 0 radians; one
cycle of a 6 Hz cosine wave (thin black line) is superimposed on the
graph.
doi:10.1371/journal.pone.0006142.g007
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in primary visual cortex is relevant to conscious experience per se,
or whether lesions of this region simply disturb consciousness by
disrupting the flow of information to higher brain regions [55].
We found that the recurrent gamma-oscillatory network
identified in this study was modulated at a theta frequency,
consistent with previous studies of endogenous oscillatory
synchronization time-locked to perceptual switching in binocular
rivalry [25]. This supports the hypothesis that theta-modulated
gamma-band synchronizations are essentially related to perceptual
experience and define discrete ‘frames’ of consciousness, consistent
with results from attentional blink experiments and those
investigating coherent perception of visual images [19,24]. The
distribution of dominance durations in our study, consistent with
findings from previous studies, suggests that perceptual switching
did not occur on every theta cycle. This indicates that the theta
cycle determines when a new perceptual experience can occur, but
that the content of each ‘frame’ of consciousness does not need to
differ from that of its predecessor (see Figure 1). For example,
continuous viewing of a single unchanging stimulus will yield a
procession of theta cycles in which the content represented on
each cycle remains the same. Since perceptual transitions are not
manifest on each theta cycle, it is apparent that some additional
mechanism is at play, and determination of what induces
perceptual transitions on particular cycles represents an important
question for future study. It seems very likely, however, that a
complete theta cycle is necessary, if not sufficient, for the onset of a
new perceptual experience. This is evidenced by the finding that
when stimuli are presented at speeds above the theta rate not all of
these stimuli would result in perceptual experience as there would
not be enough ‘frames’ to represent each one (attentional blink).
Although discreet moments of perception can only occur at a
certain rate, as demonstrated by the attentional blink phenome-
non, subjective consciousness is seamless and continuous rather
than presenting itself as a sequence of discrete conscious moments.
The results presented here suggest a similar arrangement, as
perceptual consciousness is updated by a periodic mechanism but
is experienced as a continuous and stream of consciousness. The
precise physiological mechanisms responsible for coherent transi-
tions from one conscious frame to the next and the integration of
discrete intervals into a coherent stream of conscious experiences
remain unclear. Consciousness vectors, however, analogous in
function to visual motion vectors in area V5/MT and arising from
prefrontal function, have been proposed to underlie this function
[56,57].
Illustrative of the relationship between these oscillatory
mechanisms and dominance durations is the fact that gamma-
band activation of right ITG and left PreCG occurred in the 220–
280 ms pre-response window yet was absent in the earlier 540–
600 ms pre-response interval. This suggests that it was during this
period of gamma-band synchronization that a new percept
Table 2. Summary of gamma-PLV modulation by theta phase and inter-regional interaction between theta phases.
Source PairPLV by 1st?*
PLV by 2nd?Theta-theta?Theta phase relationship
R SFG-R DLPFC YesYesYes3p/4
R DLPFC-L DLPFC No NoYes3p/4 & p/4
R DLPFC-L SFG YesYesYes3p/4
L SFG-L DLPFC NoNoYes
p/4 & 3p/4
L DLPFC-R SFGYes NoYes
p/4
L SFG-R SFGNoNoYes3p/4
R PreC-R DLPFCYesYesYes
p/4
R PreC-L DLPFC NoYesYes3p/4 & p/4
R PreC-R SFGNoNo Yes
p/4
R PreC-L SFG YesYes Yes
p/4
R SFG-R PreCG No YesYes3p/4
R DLPFC-R PreCG NoNo? Yes3p/4
L SFG-R PreCG YesYesYes3p/4
L DLPFC-R PreCG NoYesYes3p/4
R PreC-R PreCGNoYes Yes
p/4
Abbreviations: R, right; L, left; PreC, precuneus; DLPFC, dorsolateral prefrontal cortex; SFG, superior frontal gyrus; PreCG, precentral gyrus.
*Yes means significant at least at two successive theta phases; No means never significant.
PLV by 1st(2nd) indicates that PLV was modulated by the 1st(2nd) of the regions listed in the source pair. Theta phase relationship indicates the phase relationship
between theta oscillations in the two analyzed regions.
doi:10.1371/journal.pone.0006142.t002
Figure 8. Two examples of theta-theta phase relationship.
Dotted lines represent the 97.5 (top) and 2.5th(bottom) percentiles and
the dark black line indicates the mean of the surrogate distribution for
each of the 60 bins of the theta cycle. Jagged red line denotes the mean
theta phase of the source indicated on the y-axis in each bin of the
theta source indicated on the x-axis. When the mean phase was greater
than or less than the surrogate line for two or more successive bins we
considered the departure to be significant (p,0.05, two-tailed). Radians
on the x-axis are in reference to a cosine wave, which is maximal at 0
radians; one cycle of a 6 Hz cosine wave (thin black line) is
superimposed on the graph.
doi:10.1371/journal.pone.0006142.g008
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emerged since the incorporation of the ITG, known to be involved
in the processing of higher-order visual patterns, could have
integrated elements of the emerging percept into the large-scale
gamma-oscillatory neural assembly defining conscious contents
[44]. Supporting this notion are studies that used implanted
electrodes and fMRI to demonstrate that stimulus-specific
activations of inferior temporal cortex are associated with
awareness of visual stimuli similar to those used in the present
paradigm [44,45]. Moreover, activation of left PreCG only during
the 220–280 ms pre-response period suggests that the initiation of
the subsequent behavioural responses occurred during that
interval. In this view, the essential prefrontal-parietal gamma-
oscillatory network uniquely subsumed areas responsible for
processing complex visual forms and patterns (right ITG) and
areas required to initiate a response (left PreCG) during the 2220
to 2280 ms period, indicating that during this interval a new
image was incorporated into visual experience and a button press
was initiated. Significant activation of right ITG and left PreCG
was not observed in the 540–600 ms interval, presumably because
this cycle more likely does not correspond to the onset of a new
percept requiring a response, as evidenced by the average duration
of dominance periods (see Figure 3). Further buttressing this
interpretation is the finding that whereas cortical regions within
the recurrent prefrontal-parietal consciousness network tended to
show strong, statistically significant modulation of gamma
amplitude by theta phase, ITG and PreCG did not. This suggests
that these regions are incorporated into the gamma oscillatory
network only on the minority of theta cycles on which a perceptual
switch occurs and a response is required. Interestingly, right
PreCG was active in both 220–280 and 540–600 pre-response
time windows and showed evidence of theta modulation of
gamma-band phase locking with parietal and prefrontal cortex.
This modulation locking was less pronounced than was generally
observed between prefrontal-parietal and prefrontal-prefrontal
source pairs, however, and no significant theta modulation of
gamma amplitude was observed in right PreCG. As such, future
research will be required to determine what role, if any, the right
PreCG plays in perceptual transitions.
We found that both the amplitude and the inter-regional
synchronization of gamma oscillations in the identified network of
cortical regions were coupled to the phases of theta oscillations in
those same areas. This confirms that the cortical theta rhythms
modulate the periodic assembly and disintegration of gamma-
oscillatory neural coalitions time-locked to the onset of new
percepts in binocular rivalry. Interestingly, however, maximal
gamma amplitude in bilateral SFG was occurred roughly K theta
cycle (about 83 ms) out of phase with left DLPFC, PreC and ITG
(see Figure 6). This result was unexpected, given that high gamma-
band oscillations have been previously found to be maximal
during the trough of ongoing theta oscillations [31]. Our analysis,
centred within a lower 35–45 Hz frequency range, suggests that
coincident gamma activations in different cortical regions can be
locked to different theta phases. Moreover, a similar result was
found for inter-regional synchronization in the gamma band: the
synchronizations were modulated differently by theta phase in the
different region pairs, sometimes by theta phase in only one of the
regions, but also sometimes by different theta phases in the two
regions. An example of the latter is the right PreC and right
DLPFC pair, where phase locking value was maximal at a right
DLPFC theta phase of around 5p/4, whereas it was maximal at a
right PreC theta phase of about 7p/4. Importantly, the theta
phases in these two regions tended to differ by about p/4,
indicating that the gamma synchronization maxima were locked to
different theta phases each both regions. Moreover, theta phases in
all source regions tended to be locked with each other, either with
a phase difference of about p/4 or about 3p/4 (see Table 2). This
result confirms that periodic gamma synchronization is recurring
at a theta rate within regions comprising the prefrontal-parietal
‘consciousness network,’ and that the local gamma activations and
inter-regional synchronizations are modulated by theta phase, but
indicates that theta oscillations differ in phase across cortical
regions. Interestingly, left DLPFC displayed a propensity for theta
phase differences with three other regions of both p/4 and 3p/4,
suggesting that left DLPFC must be alternating between two
relatively stable and roughly equally strong phase relationships
with other areas. Beamformer source localization, together with
assessment of phase locking and instantaneous amplitude in
source-reconstructed time-series, also indicates that these regions
show recurrent coincident gamma activation and inter-regional
synchronization (see Figures 4 and 5). Thus our hypotheses are
confirmed that recurrent activation and integration of a gamma-
oscillatory network of cortical regions is time-locked to the onset of
new visual percepts in binocular rivalry, and that the formation
and dissolution of these neuronal complexes are phase-locked to
ongoing cortical theta rhythms. Our results suggest, however, that
an overarching cortical theta ‘cycle’ would in fact consist of
multiple synchronized oscillators which each maximized phase-
locked gamma activity during the same time intervals, despite
phase offsets. In order for such theta oscillations to maintain
periodic gamma activation across cortical regions, it must be the
case either that the theta oscillators are interacting across cortical
regions, or that their synchrony is maintained by some mechanism
exterior to the oscillators themselves. The finding that coincident
gamma activation within different cortical regions is locked to
different theta phases suggests that the interplay between these
slow and fast rhythms is, at least in some circumstances, more
complex than was previously imagined. Further research will be
required to better illuminate the nature and function of these
cross-frequency relationships across various experimental condi-
tions, as well as across frequency ranges within the gamma band
[see 31]. Specifically, the generality of these mechanisms will need
to be established. It is not clear how the network mechanisms
revealed by perceptual transitions during binocular rivalry
correspond to cortical dynamics across the wider context of
mental life. The temporal profile and characteristic patterns of
oscillatory synchronization during the attention blink suggest that
theta-gamma mechanisms implement independent frames of
perceptual experience, but it is not clear how such activity would
be affected by more complex and realistic perceptual conditions or
externally induced alternations in binocular rivalry. For example,
it has been shown that salient stimuli can reset the phase of theta
oscillations [58], suggesting that the timing of gamma oscillatory
mechanisms underlying perceptual experience may be affected by
environmental demands.
Interposed between recurrent gamma-band synchronizations
are periods during which gamma rhythms become relatively
desynchronized. These intervals likely play an important role in
ongoing cortical network dynamics underlying the stream of
perceptual consciousness. Transient desynchronization of gamma
oscillations has been shown to occur between periods of transient
task-relevant synchronization [19]. This process, known as ‘phase
scattering’ is understood as a mechanism by which existing task-
and/or percept-dependent neural coalitions are terminated. This
periodic dissolution of functional connectivity allows new assem-
blies of synchronously oscillating neural populations to emerge in
order to code the features of a new percept or integrate processing
elements required for new tasks. In the present study these periods,
such as the 370–430 ms pre-response interval used as the baseline
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in some of the analyses, likely play an important role in
implementing the stream of perceptual consciousness by ending
each ‘frame’ of perceptual experience. Notably, the beamformer
source localization techniques we employed here operate by
localizing the sources of activity within one time window relative to
activity in a second time window of equivalent length. Accord-
ingly, localization of 35–45 Hz activity from 2220 to 2280 ms
relative to 2370 to 2430 ms would provide the same source
solution as the opposite analysis, except with opposite valence of
activation/deactivation. Viewed through this relativistic lens, our
results demonstrate a network of prefrontal and parietal cortical
regions that cycles between gamma synchronization and desyn-
chronization, phase locked to cortical theta rhythms. We propose
that these oscillatory network dynamics provide a temporal
structure governing the emergence and abolition of discrete
moments of experience.
Electroencephalographic investigation of working memory, a
faculty integrally associated with perceptual consciousness, has
yielded three additional key findings suggestive of a fronto-parietal
network associated with theta-gamma oscillatory mechanisms that
may implement a ‘global workspace’ for the retention and
manipulation of to-be-remembered material. During the retention
interval (1) increased gamma-band activation is observed at frontal
and parietal electrodes, (2) coupling of theta-band and gamma-
band oscillations is observed at frontal and parietal electrodes, and
(3) theta-band and gamma-band synchronization is enhanced
between frontal and parietal electrodes [34,59,60]. Results such as
these, together with behavioural indices of working memory
suggestive of theta-modulated gamma-band mechanisms (gamma/
theta=individual working memory span; 40/6<7), have led to the
hypothesis that items are maintained in working memory by
assemblies of representational cell coalitions that are refreshed at a
gamma frequency during each theta cycle [see 61]. Such results
are consistent with accumulating evidence that cross-frequency
synchronization may be a key mechanism for the organization of
dynamic activity in the nervous system [62].
Interestingly, neuroimaging results are now converging on an
anatomical network relevant to general intelligence that is highly
correlated with working memory span and is centered in frontal
and parietal cortex [63]. On such evidence it could be speculated
that the conscious workspace, of which working memory is an
application, emerges from an essential fronto-parietal network that
achieves functional conjunction via theta/gamma oscillatory
mechanisms, and that this essential constellation of brain regions
is expanded to include other cortical regions specifically relevant to
perceptions and tasks permeating consciousness at that moment.
This notion is supported by the finding that attention, understood
as the gateway to consciousness, biases information for inclusion in
a large-scale gamma-synchronous network [35]. This network
workspace may allow for the flexible manipulation of information
and flexible expression of learned behaviour, considered to be one
of the cardinal cognitive attributes of conscious experience [64].
Accordingly, our data suggest that consciousness should not be
conceived as what remains when no task-relevant region
attributable to specific faculties is removed, but rather as the
integrated amalgamation of all momentarily relevant faculties into
a unitary constellation: the observer; the intentional actor.
The results detailed here are consistent with a more general
understanding of how mental representations arise from the
activity of distributed neural groups. Donald Hebb proposed that
memory traces and mental representations were implemented by
connectivity within a distributed network of neurons, and that the
selective re-ignition of this assembly would be tantamount to
recognition and/or recall [65]. This notion is supported by
evidence that the perception of a familiar object, even in a
degraded form, is also associated with both intra-regional and
inter-regional gamma-band synchronization [18,66]. The Heb-
bian outlook, coupled with a more modern understanding of
functional cortical anatomy, would predict that cortical regions
relevant to the representation of a memory would be activated and
functionally integrated during recognition and recall. Indeed, it
has been shown that recognition of a complex object is associated
with gamma-band activation in frontal, parietal and temporal
cortex, between which enhanced gamma-band phase synchroni-
zation and bidirectional causal interaction are observed [11,67]. In
light of the present results, this could be viewed as the integration
of temporal areas responsible for the processing of complex images
into the fronto-parietal gamma-oscillatory network integral to
perceptual experience. It is notable that schizophrenia, historically
considered to be a disorder of consciousness and characterized by
cognitive fragmentation, is associated with abnormal theta and
gamma band oscillatory activity during cognitive processing [see
68,69 for reviews]. The essential relationship between theta-
gamma mechanisms and consciousness is also highlighted by a
possible common neuropharmacological substrate. The bursting of
cholinergic projections to cortex from basal forebrain is found only
in wakefulness and REM sleep, central nervous system states
associated with consciousness, and theta and gamma activity are
correlated with bursting in these neurons [70]. Such results
demonstrate that gamma-band neural synchronization is a
fundamental mechanism for mental representation, and that its
disturbance results in alterations of conscious experience.
Implications for free will
Our results may also have implications for the interpretation of
what are perhaps some of the most disconcerting findings in
human neuroscience. Benjamin Libet used an ingenious experi-
mental paradigm to provide evidence that the conscious intention
to initiate a movement was substantially (approximately 300 ms)
preceded by the onset of the readiness potential, or RP, a buildup
of scalp-recorded electrical activity originating in the motor
cortices, taken to indicate the initiation of a behavioural response
[71,72]. Libet considered this to be evidence that unconscious
impulses were the true cause of action, and that the conscious
experience of intent to move occurred later and was antedated in
our experiential model of the world. The interpretation of this
result has been the subject of great debate and scrutiny. Most
damaging has been the criticism that it is not possible, at least in
any straightforward way, to compare the timing of conscious
perceptions to the timing of their external causes, such as the
perception of the stimulus that Libet used to measure the timing of
action intention [73].
Although the experimental paradigm used in the present study
was not designed to directly address the temporal relationship
between movement and the will to act, our results provide a
unique vista on the relation of gamma-band activity and
synchronization to consciousness and behaviour. Our data
indicate that gamma-band activation of left PreCG, presumably
involved in the generation of a behavioural response to a change in
consciousness, is uniquely present in the 220–280 ms pre-response
period of activation, and is notably absent in the preceding 540–
600 ms window. Moreover, left PreCG is integrated into the
prefrontal-parietal network by means of inter-regional gamma-
band phase synchronization during the same cycle that ITC is
activated and integrated into this network. These observations
suggest that initiation of behavioural responses signaling the onset
of new conscious percepts, at least as indexed by gamma-band
activity, precede action and occur at reaction times consistent with
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those observed in complex perceptual tasks. This is consistent with
evidence that gamma-band oscillations in motor cortex are
relevant to the initiation and control of movement [74]. This
means, contrary to Libet’s conclusions, that at least one neural
indicator of the timing of conscious experience is compatible with
the view that consciousness is relevant to the initiation of volitional
action. Initiation of a behavioural response coincides with
perception of a new image, indexed by activation and network
integration of ITC, indicating that conscious experience is directly
related either to the initiation of a behaviour or to the awareness of
its initiation. By relating ongoing internal processes to behaviour,
rather than attempting to correlate the internal perception of an
external event with the timing of behaviour, we have overcome a
critical confound of Libet’s paradigm. A liberal interpretation of
our results would suggest that (1) consciousness, or biological
processes directly underpinning consciousness, may indeed control
behaviour, and (2) the experience of volition is not antedated. Such
interpretations, however, are speculative as our paradigm is not
ideal for the evaluation of these hypotheses. It must also be
acknowledged that neural activity in other frequency ranges might
precede that in the gamma band, and might be more directly
related to the initiation of a voluntary response. Thus, our findings
simply suggest an intriguing avenue for future research into the
chronometry of experience and its implications for free will.
Methods
Subjects and experimental paradigm
Data were recorded from 14 subjects with normal or corrected-
to-normal vision. Subjects viewed rivaling stimuli through a mirror
stereoscope while EEG was recorded from 59 electrodes at
standard 10–10 locations plus 3 at nonstandard locations below
the inion, using an isolated bioelectric amplifier (SA Instrumen-
tation, Inc., San Diego, CA). Scalp recordings were referenced to
the right mastoid electrode. Electrodes placed above and beside
the right eye were recorded bipolarly in order to identify and
remove ocular artifacts. Impedances were kept below 15 kV
(sufficient as amplifier input impedances were .2 GV). Stimuli
were complex images (a blue butterfly on a yellow background and
orange maple leaves on a blue background, each measuring 5.3u
wide by 5.6u tall viewed at a distance of approximately 73 cm from
the eye’s nodal point) with small red circular dots in the centres
and white borders surrounding each image to maintain and judge
alignment (see Figure 1). Contrast and luminance were chosen
from a palette to yield approximately equal full dominance
intervals for the two percepts and were relatively high (standard
colours in Adobe Illustrator ?). These stimulus parameters yielded
a modal full dominance interval around 550 ms.
Subjects were seated and a chin rest was used to maintain head
position throughout the experiment. Subjects were instructed to
depress buttons using two fingers on their right hand to indicate
which of the rivaling images, if any, completely dominated
perception at any given time. Specifically, subjects were instructed
to depress button 1(2) to signal onset of dominance for left(right)
eye stimulus, continue to hold down button 1(2) as long as the
left(right) eye stimulus dominated, and to release button 1(2) to
signal loss of perceptual dominance for left(right) eye stimulus.
This produced a continuous record of the onset and offset of
periods of perceptual dominance. Prior to recording, subjects
received training to identify periods of complete dominance and to
check the alignment on left and right eye stimuli. After training,
subjects performed in 12 blocks lasting 4 minutes each. Between
each block subjects were given the opportunity to rest, after which
they were presented with a screen directing them to check the
alignment of the stimuli before commencing the next block. Rest
and the realignment periods were terminated by responses from
subjects. EEG data were filtered at 0.1–100 Hz, amplified with a
gain of 20,000, digitized at 500 Hz, and stored for off-line analysis.
All subjects gave written informed consent before participating in
the experiment. The protocol was approved by the UBC
Behavioural Research Ethics Board.
After the data were recorded, behavioural indices of perceptual
switching were computed to determine the number of epochs of
stable perceptual dominance lasting 700 ms or longer. Epoch
length was defined as the time between a button press signaling the
onset of a period of complete perceptual dominance by one of the
two images and the release of that button signaling the termination
of complete perceptual dominance by that image. An interval of
complete perceptual dominance was defined as a period wherein
the perception of one stimulus was uninterrupted, either by
perception of the other stimulus or by an ambiguous percept
containing elements from both images. Subjects who did not
display stable patterns of rivalry during their first session were
excluded from the study. Subjects who did display stable patterns
of rivalry but lacked a sufficient number of stable percepts for
analysis were asked to return for a second, and if necessary, third
recording session. Ten of the 14 subjects displayed a pattern of
stable periods of complete perceptual dominance and their data
were retained for further analysis.
Beamformer source localization
Epochs time-locked to button presses signaling the onset of a
new stable percept were extracted from 1300 ms prior to the press
until 300 ms after it. Stable percepts were defined as those lasting
700 ms or longer. Epochs containing ocular and nonocular
artifacts were rejected using the automated artifact rejection
algorithm implemented in the Brain Electrical Source Analysis
software suite (BESA 5.2; Megis Software). One subject’s data
were excluded from analysis because of excessive contamination
by artifacts. Data from the remaining 9 subjects were used for the
subsequent electrophysiological analysis (mean age 23.3; 3 female).
Data from these subjects yielded 3281 epochs of stable perceptual
dominance with approximately equal incidence of left eye and
right eye dominance (1805 left eye; 1476 right eye).
Scalp data for individual participants were transformed into the
time-frequency domain from 10 to 60 Hz using the complex
demodulation procedure implemented in BESA with a time-
frequency sampling of 5 Hz/10 ms [see 75]. Time windows of
interest were selected by averaging the time-frequency data across
participants and across a subset of electrodes that encompassed the
fronto-parietal regions where theta-modulated gamma-band
activity was expressed most clearly (F1, F3, F5, F2, F4, F6, FC1,
FC3, FC5, FC2, FC4, FC6, C1, C3, C5, C2, C4, C6, CP1, CP3,
CP5, CP2, CP4, CP6, P1, P3, P5, P2, P4, P6). The lowest gamma
power occurred approximately 400 ms pre-response, with peaks of
gamma activity in the 35–45 Hz range occurring on either side of
this power decrease at approximately 220–280 ms and 540–
600 ms pre-response (see Figure 3). The topographical distribution
on the scalp of the 35–45 Hz activity in each of the two time
intervals of interest were plotted, relative to the amplitude of the
activity in the same frequency band during the baseline period, in
Figure 3a. Increases in intra-regional gamma-band synchroniza-
tion were widely distributed over the scalp, largely over frontal,
central and parietal scalp sites.
To identify cortical loci expressing intra-regional gamma-band
synchronization time-locked to button presses indicating percep-
tual switching, the Multiple Source Beamformer implemented in
BESA was applied to data from each subject using a standard
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realistic head model. This method has been demonstrated to be
effective for localization of sources of oscillatory activity within
highly specific time-frequency windows [76]. Beamformer analysis
estimates the contribution of a given voxel in the brain to activity
recorded on the scalp within a specified time-frequency window by
minimizing contributions from all other voxels in source space,
thereby implementing a spatial filter to identify neural generators
of scalp activation [77,78]. This analysis requires a baseline period
of the same duration as the time window of interest. Therefore we
applied the beamformer to 35–45 Hz activity occurring 220–
280 ms and 540–600 ms pre-response, relative to an intervening
370–430 ms baseline in the same frequency range. Beamformer
source reconstructions were obtained separately for each partic-
ipant in each of the time intervals of interest. Non-parametric
statistical analysis was then performed using functional neuroim-
aging analysis software (AFNI) [79]. Statistically significant (p,.05
or greater) sources of activity were then displayed on a three-
dimensional rendered standard brain. The statistical results
indicated the presence of bilateral generators in both DLPFC
and SFG. Due to the proximity of the prefrontal sources, however,
it was unclear whether there were actually four distinct source
locations or if any of the statistically significant sources reflected
the spread of activity from nearby neighboring sources. To ensure
that we were accurately identifying source locations for the
subsequent PLV analyses, we examined the average beamformer
output for all participants, without statistical analysis, confirming
that the DLPFC and SFG sources were distinct from one another.
Ambiguity of statistical significance for reasons of source proximity
or rendering orientation was apparent in the group surface-
rendered data in the cases of the right DLPFC and left DLPFC in
the 540–600 ms window and left SFG in the 220–280 ms window
(see Figure 4). In these cases, it was unclear whether these foci of
gamma identified activity in source space were producing
statistically significant activation on the surface-rendered image,
or if the spread of significant activation attributable to only one
source. To confirm that each of these sources was significant, the
voxel representing peak activation for each source in question was
subjected to statistical analysis (see Table 1). While useful in
resolving such scenarios of ambiguity, the approach of testing peak
voxels was not employed as a primary assessment because (1) it
does not provide an accurate representation of the anatomical
spread of the generator, thereby obfuscating the functional
significance of the cortical source, and (2) it would require the
added assumption that activity of the peak voxel was essentially
similar to that of adjacent cortex.
Inter-regional phase locking
In order to assess synchronization within and between cortical
sources of gamma-band activation time-locked to perceptual
switching in binocular rivalry, we extracted epoched broadband
time series using a source montage in which locations were
assigned to coordinates of all activational peaks for statistically
significant sources (Table 1; BESA 5.2; Megis Software). Notably,
the algorithm we employed creates a spatial filter for each source
that excludes contributions from any other modeled sources, as
well as limiting the contributions of noise and non–modeled
activity to the source activity [see 80 for algorithm]. The sources
thus are equivalent to virtual electrodes in the brain with
approximately 3–4 cm diameter [80]. Epoched broadband signals
computed from the modeled sources were band-pass filtered
digitally at 1 Hz intervals Hz (passband=f60.05f, where f
represents the filter frequency). We then calculated the analytic
signal
z t ð Þ~f t ð Þzi~f f t ð Þ~A t ð Þeiw t ð Þ
of the filtered waveform for each epoch, f(t), where~f f t ð Þ is the
Hilbert transform of f(t) and i~
phase, w(t), and amplitude, A(t), at each sample point. Envelope
amplitudes obtained in this manner and standardized as described
in the next paragraph were used as indices of intra-regional neural
synchronization.
We measured inter-regional phase synchronization by calculat-
ing phase-locking values. PLVs were computed from the
differences of the instantaneous phases for pairs of time series
from the reconstructed gamma-band sources, for example, sources
j and k, at each point in time, t, across the N available epochs [81]:
ffiffiffiffiffiffiffiffi
{1
p
, to obtain the instantaneous
PLVj,k,t~N{1X
N
ei wjt ð Þ{wkt ð Þ
½?
?????
?????
PLVs take on values between 0 (random phase difference, no
phase locking) and 1 (constant phase difference, maximum phase
locking). Our goal was to characterize inter-regional gamma-band
synchronization occurring during periods of gamma activation
time-locked to button presses indicating perceptual switching,
relative to intervening phases of relative gamma desynchroniza-
tion. This approach was employed to directly test the hypothesis
that windows of gamma activity correspond to structured,
synchronously oscillating neural ensembles corresponding to the
construction of integrated experiences, whereas interposed desyn-
chronizations reflect network dissolution. Accordingly, PLVs were
calculated for each time point in the 220–280 ms and 540–600 ms
windows. These values were standardized relative to the
intervening 370–430 ms baseline. Standardization was accom-
plished by subtracting the mean baseline PLV from the PLV for
each data point and dividing by the standard deviation of the
baseline PLV. The resulting PLVzscores indicate standardized
changes from the average baseline PLV.
To assess the statistical reliability of changes from baseline in
inter-regional synchronization and desynchronization we em-
ployed the surrogate statistical method [81]. To this end we
scrambled the epochs and computed PLVs for the scrambled data
for each frequency and time point combination for each pair of
sources. The resulting PLVs were then standardized relative to the
(scrambled) 370–430 ms pre-response baseline. This process was
repeated 200 times to create a surrogate distribution for the
relevant standardized PLV. The percentile rankings of real data
from the normalized PLV values within the surrogate distributions
were used to assess the statistical significance of observed changes
in synchronization. A change in gamma-band synchronization was
considered to be significant between a pair of cortical regions
activated in either the 220–280 ms or 540–600 ms time windows
at p,0.01 (two-tailed) if the real PLV was higher than all 200 data
surrogates, and significant at p,0.05 (two-tailed) if the real PLV
was greater than 195 of the data surrogates. To ensure confidence
and conservatism in the reporting of these results, synchronizations
were required to persist for a minimum of 25 ms (one cycle at
40 Hz and 12 data points at the 500 Hz sampling rate) and
encompass multiple frequencies within the specified time-frequen-
cy window to be considered significant. Furthermore, in rare cases
where significant desynchronization was found within the same
time-frequency window as synchronization, the synchronization
was not reported. The frequency window for assessment of inter-
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Page 13

regional synchronization encompassed the 30–45 Hz frequency
range, as the overall pattern of gamma-band synchronization was
concentrated in that window (see Figure 5), although many
individual source pairs were synchronized in the 35–45 Hz range
used in the beamformer analysis.
Theta modulation of gamma amplitude and inter-
regional phase locking
To test the hypothesis that gamma-band activations were
modulated by the phase of ongoing theta oscillations, cross-
frequency coupling between theta phase (6 Hz) and gamma
amplitude (40 Hz) was analyzed for each of the eight sources
identified using beamformer analysis. Theta phase and gamma
amplitude were obtained using digital filtering and the Hilbert
transform, as described above, for a period beginning 1000 ms
prior to button presses indicating the onset of a new period of
perceptual dominance and ending with the button press. This
provided time series data for theta phase and gamma amplitude
for each analyzed epoch. Values in the cross-frequency analysis
were not standardized relative to the baseline period. Gamma
instantaneous amplitude was sorted according to theta phase,
which was divided into 60 bins of 0.105 radians width, and mean
gamma amplitude within each phase bin was calculated. The
statistical significance of modulation of gamma amplitude by theta
phase was tested by calculating a surrogate distribution obtained
by creating 1000 sets of randomly-shuffled theta-phase time series
and computing the mean gamma amplitudes within each phase
bin in the same way. Modulation of gamma amplitude by theta
phase was considered statistically significant (p,0.05, two-tailed) if
the mean gamma amplitude was above the 97.5thpercentile, or
below the 2.5th
percentile of amplitudes in the surrogate
distribution for at least two adjacent bins.
Assessment of the modulation of inter-regional gamma-band
phase locking was accomplished in a similar manner. The Hilbert
transform was used to obtain the phases of non-normalized 40 Hz
and 6 Hz signals from pairs of sources during 1000 ms epochs
preceding button presses indicating the onset of a new perceptual
dominance period. For each analyzed source pair, epochs were
sorted according to the theta phase of one of the sources. This
produced 60 bins, each 0.105 radians in width, and each
containing 27,342 pairs of gamma phases for each source ((3281
epochs6500 time points)/60 bins). PLVs were then calculated in
the manner described above within each bin, producing an index
of the amount of gamma-band phase synchronization between a
pair of sources typical during a particular segment of ongoing theta
oscillations in one of the analyzed sources. Statistical significance
was assessed by creating a surrogate distribution of 1000 sets of
shuffled theta-phase time series and calculating gamma-band PLV
in each phase bin in the same way. We considered modulation of
inter-regional gamma-band phase locking by theta phase to be
statistically significant (p,0.05, two-tailed) if the PLV was above
the 97.5thpercentile, or below the 2.5thpercentile of the surrogate
distribution for at least two adjacent bins.
The relationship between theta phases in pairs of brain regions
was analyzed for the same 1000 ms epochs similarly to the analysis
of the theta phase-gamma amplitude coupling. For theta phase,
the epochs were sorted by the theta phase of one of the two regions
in a pair, 60 bins 0.105 radians in width were created, and the
mean theta phase in the other region was calculated for each bin.
Statistical significance was assessed by creating a surrogate
distribution of 1000 sets of shuffled theta-phase time series for a
given region and calculating mean theta phase for the other region
in each phase bin in the same way. We considered modulation of
theta phase in one region by theta phase in another region to be
statistically significant (p,0.05, two-tailed) if the mean theta phase
was above the 97.5thpercentile, or below the 2.5thpercentile of the
surrogate distribution for at least two adjacent bins.
Acknowledgments
We thank Stephanie Tha ´i and Alan Rahi for their help in the recording
and analysis of the data. We also thank Dr Keiichi Kitajo, RIKEN Brain
Science Institute, and Dr Kentaro Yamanaka, University of Tokyo, for
help in developing the phase synchrony analysis programs.
Author Contributions
Conceived and designed the experiments: SMD JM LW. Performed the
experiments: SMD LW. Analyzed the data: SMD JJG LW. Wrote the
paper: SMD JJG LW.
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