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Available online at www.sciencedirect.com

ScienceDirect
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Brain oscillations in perception, timing and action

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Daya S Gupta1 and Lihan Chen2,3

Catching a thrown ball requires a tight coupling between
perception and motor control. In this review, we examine
multidimensional information processing across various
perceptual and motor tasks. We summarize how perception,
timing and action can be understood in terms of the coupling of
gamma band oscillations, which represent the local activities of
brain circuits, to a specific phase of long-range low-frequency
oscillations. We propose a temporal window of integration that
emerges from cross-frequency coupling that serves to produce
optimized action.
Addresses
1
Department of Biology, Camden County College, Blackwood, NJ
08012-0200, USA
2
Department of Psychology and Beijing Key Laboratory of Behavior and
Mental Health, Peking University, Beijing 100871, China
3
Key Laboratory of Machine Perception (Ministry of Education), Peking
University, Beijing 100871, China
Corresponding authors: Gupta, Daya S (dayagup@gmail.com) and
Chen, Lihan (CLH@pku.edu.cn)

Current Opinion in Behavioral Sciences 2016, 8:xxyy

This review comes from a themed issue on Timing behavior
Edited by Richard B Ivry and Warren H Meck

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http://dx.doi.org/10.1016/j.cobeha.2016.02.021
2352-1546/# 2016 Elsevier Ltd. All rights reserved.

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Introduction
To hit a pitched baseball requires that the batter generates
accurate estimates of the position, speed, and timing of the
moving ball and use this information to produce a coordinated movement. Humans are adept in compensating for
their own sensorimotor uncertainty in the execution of
skilled actions [1,2,3]; however, the neural mechanisms
underlying the temporal coordination between perception
and action have not been fully established.
Different lines of evidence have facilitated our understanding of the computations and physiological underpinnings that are involved in the coupling of perception
and action. For example, a recent computational modeling study revealed that the internal representations of
observers spatial visuomotor errors (in visuomotor decision tasks) are best described by a mixture of distributions
that differ in location and scale [2]. This indicates that
the internal probability density functions of their own
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visuomotor error distributions are discrete [2]. These

results suggest that discrete neurophysiological processes
may be responsible for various sensorimotor tasks. In this
review, we propose that the processing of multidimensional information by neuronal populations occurs in
separate epochs and that these epochs represent different
facets of the interaction between perception and action
(Figure 1).

Multidimensional processing of sensorimotor

information
Over the last decade, there has been considerable interest
in the roles of cross-frequency phase-amplitude coupling
in various cognitive functions [4]. Cross-frequency
phase-amplitude coupling is a phenomenon in which
the phase of a lower frequency brain oscillation modulates
the amplitudes, i.e., the differences in the maxima and
minima of oscillation waves, of a higher frequency oscillation to create packets of those higher frequency waves
[4]. Coupling of the phases of low-frequency theta (4
8 Hz) and alpha (812 Hz) oscillations to the amplitudes
of high-frequency gamma (30150 Hz) oscillations
[5,6,7,8,9,10,11,12,13,14,15] has been observed in various sensory and motor tasks. In one study, visual processing is found to reflect local activity, whereas working
memory retention and mental imagery, which likely involve multiple, distributed cortical areas, are related to
theta (48 Hz) and alpha (812 Hz) frequency oscillations
[11]. Furthermore, gamma band neuronal oscillations that
relate to the spiking activities of neurons [9,15,16] in
response to stimulus characteristics, including intensity
and duration, have been observed in many cortical and
subcortical structures [17,18,19,20,21]. Additionally, a recent study demonstrated zero and non-zero lags between
the phases of gamma oscillations in spatially separate sites
in the primary visual cortex [22]. These non-zero lags are
modulated by the stimulus, suggesting that gamma oscillations can also dynamically influence the exchange of
information among local populations of neurons [22].
In contrast to gamma oscillations, low-frequency oscillations generally synchronize larger areas of the cortex and
play a role in long-range interactions [4,15]. Thus, as a
result of phase-amplitude coupling, gamma-band oscillations reflect local activities, whereas low-frequency oscillations help to engage their long-range interactions
[4,15]. In the framework of multidimensional processing, the amplitudes of high-frequency oscillations that
synchronize the processing of information in multiple
local circuits are modulated by the phases of synchronous
long-range low-frequency brain oscillations. This phaseamplitude coupling causes information to be coherently
Current Opinion in Behavioral Sciences 2016, 8:xx

Please cite this article in press as: Gupta DS, Chen L: Brain oscillations in perception, timing and action, Curr Opin Behav Sci (2016), http://dx.doi.org/10.1016/j.cobeha.2016.02.021

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COBEHA 203 XX

2 Timing behavior

Figure 1

Local circuits
(Fast Oscillations)
Buzsaki G, Watson BO: Dialogues Clin Neurosci (2012)

Working Memory
Multimodal
Motor

Sensory

Pre
tal

fron

CORTEX

(a)

Multidimensional Processing of Information

(Low-frequency Oscillations)
Local spiking activity
is coupled to a-phase
of the fast oscillation
ISI = 30 ms
Belitski A, et al: J Neurosci (2008) 28(22):5696-5709

t1

t2

t3

Fast Oscillations

TWI

Local Circuits

Less Information

~50200 ms

ISI = 60 ms

t1

t2

t3

Low-frequency Oscillations
(~520 Hz) Multidimensional

More Information

Processing
(c)

(b)

Shannon Information
Current Opinion in Behavioral Sciences

Schematic depiction of the multidimensional processing of information in the brain.

(a) Activities in local circuits are modulated by the phase of long-range low-frequency oscillations (indicated by curved lines spanning a large area
of the cortex). Sensory, motor, multimodal and association areas in the prefrontal cortex (oval boundaries) are shown as examples of local circuits.
(b) Depicts cross-frequency phase-amplitude coupling. Note that multiunit spike bursts (shown inside a circle) have been observed in experimental
studies to exhibit a dependency on the phase of fast (gamma band high-frequency) oscillations. t1, t2 and t3 are time points, present at intervals
that equal the periodicity of low-frequency oscillation, when fast oscillations synchronize activities (spike bursts) of local circuits. Multidimensional
information processing occurs as a result of the modulation of fast oscillations (synchronizing local circuits) by long-range low-frequency
oscillations. The phase of low-frequency oscillation when spike bursts in local circuits are synchronized by fast oscillations will provide the
temporal window of integration (TWI) of stimuli. Spike bursts contain information (see panel c) that is processed in the multidimensional domain
during a sensorimotor task.
(c) Interstimulus intervals (ISIs) between two frames of a Ternus display, which is a special case of apparent motion [52], are processed differently
depending on the length of the ISI to produce different content levels of Shannon information. Notice that there is less uncertainty regarding the
presence of spikes in time-bins of the same length that contain shorter ISIs, i.e., the information content is relatively reduced. The shorter ISIs,
with less information content, are associated with the percept of element motion, which contrasts with the group motion observed with the longer
ISIs.

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COBEHA 203 XX

Oscillatory structures in the brain Gupta and Chen 3

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processed in distributed circuits, supporting the tight

temporal coupling between various aspects of a sensorimotor task. The degree of this coupling depends on the
demands of the task. For example, catching a fastermoving object requires a tighter coupling between various sensorimotor functions that occurs over shorter subsecond durations.
The information resulting from the activities of local
circuits can be described by Shannon entropy, i.e., the
amount of uncertainty about whether a neuron that represents an information source, such as the primary visual
cortex, will or will not fire within a particular temporal
window [23,24]. Information or entropy in the proposed
multidimensional domain is a consequence of the stochastic nature of the neuronal responses to a stimulus
[25,26,27]. Other sources of information for multidimensional processing may include higher functional areas, such
as the somatosensory areas, multimodal areas, motor areas
and the anterior association area in the prefrontal cortex.
Note that the information resulting from the coherent
neuronal activities that are responsible for sensorimotor
tasks can be quantified by different analyses, including
wavelet information analysis and the study of spike structures in terms of complexity and randomness [26,27,28].
In one study in which primates were presented with naturalistic scenes, a positive correlation was observed between
high-gamma local field potential (LFP) (60100 Hz) and
spikes, along with a strong positive correlation within highgamma LFPs in the primary visual cortex [16]. These
findings suggest that high-gamma LFPs and spikes are
generated within the same network [16]. Another study
revealed significant phase correlations in approximately
60% of the multiunit activities of neurons and LFP recordings from visual cortices during a specific visual stimulation
in addition to phase correlations between oscillatory events
at different frequencies [15]. As such, the information in
spike structure [27] during multidimensional processing is
indicative of sensorimotor responses.
It was observed that stimulus-driven excitability variations
in local cortical ensembles are related to the phases of brain
oscillations within the setting of a hierarchical cross-frequency coupling amplitude of a higher frequency
oscillation is coupled with the phase of a lower frequency
oscillation [29,30]. Accordingly, we propose that synchronized long-range low-frequency oscillations provide a temporal window of integration (TWI) in the framework
multidimensional processing. The TWI may manifest as
a peak or trough of a low-frequency brain oscillation
because coupling has been observed between the high
gamma power and the peak phases of alpha (812 Hz)
oscillations in a working memory task [31] and the troughs
of theta (48 Hz) oscillations in motor, sensory and cognitive tasks [5]. Moreover, the TWI is likely to be related to
the periodicity of the low-frequency oscillations. Typical
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integrations of auditory and visual events occur within a

time window of 100 ms, for example, those observed
during the sound-induced double-flash illusion [32]. The
sound-induced double-flash illusion may be explained by
the coupling of the activities of the auditory and visual
circuits to the same phase of a slow wave oscillation in the
framework of multidimensional processing. An important
supporting piece of evidence comes from spatial ventriloquism in which a visual object can attract the perceived
location of a spatially discordant but temporally synchronous sound [33,34]. This attraction can be understood as a
phase-amplitude coupling of the circuits processing the
sound to the synchronized low-frequency oscillations that
are devoted to processing different features of the visual
object.
Although spatial ventriloquism is an example of the
integration of spatially separate events, phase-amplitude
coupling is observed in the integration of information
associated with inputs arising from a single source. For
example, during simple visual tasks, alpha/high gamma
coupling preferentially increases in the visual cortical
regions [8]. A recent study provides the causal evidence
that the temporal window of integration associated with
sound-induced double-flash illusion is constrained by the
frequency of occipital oscillations in the alpha band [34].
Faster alpha frequencies also predict vision with a finer
temporal resolution, which is consistent with the hypothesis that faster alpha oscillations provide more cycles for
the separate rather than combined integration, which
results in better resolution [35].
In another study of the integration of two stimuli (i.e., audio
and tactile), the alpha power recorded over the superior and
inferior parietal lobules was relatively increased in a pretactile stimulus time-window of approximately 330 ms
prior to the subsequent perception of an integrated rather
than segregated stimulus [36]. Due to the lack of a poststimulus effect in this study, the integrated/segregated
perception was likely an effect of a network comprising
multisensory integration areas with unisensory areas rather than a specific multisensory area [36]. This interpretation is consistent with the multidimensional processing of
auditory and tactile stimuli within a network.
The increase in alpha power during the integration of two
stimuli can be understood in terms of multidimensional
processing. For multisensory integration to occur, the alpha
oscillations modulating both unisensory circuits, i.e., tactile
and auditory, must synchronize, producing an increase in
alpha power. Therefore, one may argue that the processing
of multiple sensory stimuli (as depicted in Figure 1) within
successive but discrete TWIs results in the integration of
sensory information from multiple sources in a dynamic
network of circuits over a time period. This integration
forms the basis of successful sensorimotor interactions with
the external physical environment.
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Multidimensional processing in apparent

visual motion
In this section, we argue that pre-stimulus alpha power
and spontaneous brain oscillations influence apparent
motion perception [37]. Apparent motion is a visual
illusion in which motion is perceived when two spatially
distinct static objects alternate in sequence. Apparent
motion illusions are robust at presentation frequencies
of approximately 3 Hz. Apparent motion has been
deemed to be dependent on the ability to use predictive
feedback signals in the processing of fragmented sensory information [38,39]. The perception of good apparent
motion follows an optimal range of presentation frequencies. Lower alpha power predicts percepts between apparent motion and flickering at high presentation
frequencies. In a study, higher alpha power predicts
apparent motion percepts of visual objects with low
presentation frequencies [37]. Specifically, apparent motion perception depends on both local neural synchronization (i.e., the power within the frontal and occipital
regions of interests) and long-distance neural synchronization (i.e., frontal-occipital connectivity) in the pre-stimulus alpha oscillations [37].

Multidimensional processing in timing and

action
Phase-amplitude coupling provides a plausible mechanism
for the calibration of modular clocks. This calibration
involves endogenous oscillators within various networks,
modules that calibrate the oscillators, and downstream
circuits that process task-specific time intervals. These
components are connected via flexible connections as
proposed by Gupta (2014) [40]. The modular clock mechanism is calibrated by circuits, such as those in the cerebellum and posterior parietal cortex, which are important
for feedback control during various sensorimotor tasks
[40]. During complex sensorimotor tasks, such as catching
a flying ball or lifting a cup, irregular spike bursts are
produced during feedback processes and reflect unequal
temporal epochs that separate the activities of individual
muscles during these movements. Furthermore, the irregular changes in the neuronal activities during a sensorimotor task mirror the changes in the physical time-related
parameters, such as speed and duration. The input from
feedback circuits to endogenous oscillatory mechanisms
aid in the transfer of the physical time information. Note
that phase-amplitude coupling preserves the temporal
relationship between the parallel inputs of irregular activities that arrive at the oscillator/local clock mechanism from
a calibration module. Additionally, motor and sensory taskmodulated changes in the activities of neurons are observed in parts of the brain, such as the inferior temporal
lobe and prefrontal cortex, which are not directly responsible for the feedback control of external sensorimotor tasks
[41,42]. These changes may influence the effects of feedback processes and could also be responsible for the
calibration of endogenous oscillators.
Current Opinion in Behavioral Sciences 2016, 8:xx

Several recent studies have also suggested the role of beta

band oscillations in the representation of various time
durations in the brain [43,44,45]. Interestingly, in a
recent study by Bartolo and Merchant (2015), putaminal
LFPs were recorded in monkeys that were performing a
synchronization-continuation task. The LFPs exhibited
an initial burst of beta band oscillation that was followed
by another increase during the continuation phase of the
task [45]. This latter increase depends on internally
generated cues [45]. The dependence on internally
generated cues suggests the involvement of other calibration modules, such as those arising from the basal
ganglia circuit as previously proposed by Gupta (2014)
[40], which may be responsible for the observed increase
in the beta power via an increase in the number of longrange beta-oscillation interactions during the continuation phase of the task.
Consistent with the role of low-frequency oscillations in
the modulation of the amplitudes of high-frequency
oscillations by long-range oscillations, previous studies
utilizing motor tasks have demonstrated phase-amplitude
coupling between movement-selective high gamma and
alpha oscillations in humans [14] and between gamma
and theta oscillations in the motor cortical areas of rats
during distinct movement states [12]. Another study
suggests a saccade-related phase-amplitude coupling between theta and low gamma activities [13]. Thus, the
amplitudes of gamma oscillations in motor areas, which
represent motor information including the time of the
onset, performance and execution [46,47], nested within
the low-frequency oscillations are likely to play an important role in the processing of information for the
execution of sensorimotor tasks.
A recent study simultaneously recorded neuronal activities
in multiple cortical regions in monkeys that were trained to
report the color or motion of the stimuli. This study
revealed complex dynamics of information flow [48]. When
information reaches one part of the brain from another, the
phase of the synchronized low-frequency oscillations connecting the two regions is advanced [49]. This delay in
phase affects the processing of the arriving information by
altering the available size of the TWI. The effect of longrange oscillations on information flow has been indicated
by an analysis of intracranial EEG data that revealed that
power changes in different frequency bands significantly
contribute to the late components of the event-related
potentials [50]. The micro-stimulation of V1 (i.e., the
primary visual area) generates gamma oscillations in the
feedforward direction, whereas such stimulation of V4 (i.e.,
a downstream visual area) generates alpha oscillations in
the feedback direction [49]. These findings suggest that
during the multidimensional processing of visual information, the coupling of the amplitude of gamma oscillations
(produced by feedforward activity) to the phase of lowfrequency oscillations (produced by feedback activity)
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Oscillatory structures in the brain Gupta and Chen 5

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could also modulate the flow of information between lower

and higher visual areas. Thus, phase-amplitude coupling
could form one of the important bases of sensorimotor
choices in flexible visuomotor tasks; such choices are
believed to result from the integration of opposite flows
of sensory and task information [48].

Summary
VanRullen and Koch (2003) proposed that cross-frequency interactions between gamma and alpha oscillations
constrain perception [51]. We extend this proposal to
include motor functions to understand the role of the
multidimensional processing of information during sensorimotor tasks. The multidimensional processing provides an important basis for understanding how different
circuits of the brain can be temporally coupled during
various sensorimotor tasks.

Conflict of interest statement

Nothing declared.

Acknowledgements
Q2 This study was supported by grants from the Natural Science Foundation of

China (31200760), the National High Technology Research and

Development Program of China (863 Program, 2012AA011602) and the
Fund for Fostering Talents in Basic Science (J1103602) to LC. DSG would
like to acknowledge his gratitude to the students, faculty and staff of
Camden County College, New Jersey, USA and the ResearchGateTM
community.

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Current Opinion in Behavioral Sciences 2016, 8:xx

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Please cite this article in press as: Gupta DS, Chen L: Brain oscillations in perception, timing and action, Curr Opin Behav Sci (2016), http://dx.doi.org/10.1016/j.cobeha.2016.02.021

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