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Power modulation of electroencephalogram mu and beta frequency depends on perceived level of observed actions

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Brain and Behavior
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Introduction The ability to understand actions and intentions of others is of great importance to social relationships and is associated with the mirror neuron system of the human brain. Whether conscious perception of specific actions is necessary to trigger activity in this system, or alternatively whether this response is independent of conscious perception is not known. Methods We addressed this issue by rendering videos of right hand movements invisible to conscious perception, and measuring electroencephalogram (EEG) power suppression in the mu (8–13 Hz) and beta (15–25 Hz) range as index corresponding to the magnitude of mirror neuron activity. Results In the beta range over bilateral sensorimotor sites, we find that suppression indices follow the reported perceptual level of subjects with stronger suppression for consciously perceived trials. Furthermore, in the nonperceived trials, oscillation power is significantly suppressed relative to baseline. In the low mu range (8–10 Hz), oscillation power over the left sensorimotor site is significantly more suppressed in the consciously perceived versus nonperceived trials. Conclusions Our data suggest that the intensity of mirror system responses during action observation decreases with the observers' perception level yet remains significant during observation of invisible actions. Such subliminal activity could help explain phenomena such as covert imitation.
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Power modulation of electroencephalogram mu and beta
frequency depends on perceived level of observed actions
Shiri Simon
1,2
& Roy Mukamel
1,2
1
Sagol School of Neuroscience, Tel-Aviv University, Tel Aviv 6997801, Israel
2
School of Psychological Sciences, Tel-Aviv University, Tel Aviv 6997801, Israel
Keywords
Action observation, conscious perception,
electroencephalogram, mirror neuron system
Correspondence
Roy Mukamel, School of Psychological
Sciences, Tel-Aviv University, Tel Aviv,
6997801, Israel.
Tel: 972 3 640 7246; Fax: 972 3 640 6390;
E-mail: rmukamel@post.tau.ac.il
Funding Information
Yosef Sagol Scholarship for Neuroscience
Research, Sagol School of Neuroscience
fellowship, I-CORE Program of the Planning
and Budgeting Committee and The Israel
Science Foundation (Grant/Award Number:
“51/11”) Human Frontiers Science Project
(HFSP) Career Development Award (Grant/
Award Number: “CDA00078/2011-C”) The
Israel Science Foundation (Grant/Award
Number: “2043/13”, “1771/13”).
Received: 3 February 2016; Revised: 11 April
2016; Accepted: 16 April 2016
Brain and Behavior, 2016; 0(0), e00494,
doi: 10.1002/brb3.494
Abstract
Introduction: The ability to understand actions and intentions of others is of
great importance to social relationships and is associated with the mirror neu-
ron system of the human brain. Whether conscious perception of specific
actions is necessary to trigger activity in this system, or alternatively whether
this response is independent of conscious perception is not known. Methods:
We addressed this issue by rendering videos of right hand movements invisible
to conscious perception, and measuring electroencephalogram (EEG) power
suppression in the mu (813 Hz) and beta (1525 Hz) range as index corre-
sponding to the magnitude of mirror neuron activity. Results: In the beta range
over bilateral sensorimotor sites, we find that suppression indices follow the
reported perceptual level of subjects with stronger suppression for consciously
perceived trials. Furthermore, in the nonperceived trials, oscillation power is
significantly suppressed relative to baseline. In the low mu range (810 Hz),
oscillation power over the left sensorimotor site is significantly more suppressed
in the consciously perceived versus nonperceived trials. Conclusions: Our data
suggest that the intensity of mirror system responses during action observation
decreases with the observers’ perception level yet remains significant during
observation of invisible actions. Such subliminal activity could help explain
phenomena such as covert imitation.
Introduction
As social beings we constantly interact and communicate
while relying on our ability to understand the actions and
intentions of others. This ability is of great importance
for survival and is associated with the Mirror Neuron
System of the brain. Mirror neurons are a particular class
of visuo-motor neurons that discharge not only when
executing an action but also when passively observing a
similar action being executed by someone else (monkey
or human) (Cattaneo et al. 2009; Rizzolatti and Sinigaglia
2010). These neurons were originally discovered using
single-cell recordings in sector F5 of the ventral premotor
cortex of macaque monkeys (Dipellegrino et al. 1992;
Gallese et al. 1996; Rizzolatti et al. 1996). Since the
original discovery, the existence of mirror neurons in
other regions of the human and nonhuman motor
pathway (including parietal, and primary motor cortex)
has been demonstrated (Filimon et al. 2007; Tkach et al.
2007; Chong et al. 2008; Dushanova and Donoghue
2010; Mukamel et al. 2010; Kilner and Lemon 2013;
Vigneswaran et al. 2013).
Physiological studies in primates have shown that simi-
lar sensory input (e.g., a hand reaching behind a screen
obscuring its end point) evokes differential mirror neuron
activity depending on context (e.g., whether there is an
object behind the screen or not) (Umilta et al. 2001).
Additionally, during observation of similar actions, mirror
ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
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Brain and Behavior, doi: 10.1002/brb3.494 (1 of 11)
neurons in inferior parietal lobe (IPL), inferior frontal
gyrus (IFG), and ventral premotor cortex, have been
shown to respond differentially depending solely on the
goal of the action (Fogassi et al. 2005; Iacoboni et al.
2005). The idea that fronto-parietal mirror neurons code
the goal of an action rather than the action’s low-level
kinematics is further supported by a study of Umilta and
colleges, showing that different actions having the same
goal evoke similar neural response (Umilta et al. 2008).
Mirror neurons have also been shown to respond not
only to visual input but also to auditory cues associated
with motor acts [e.g., the sound of breaking a peanut
(Kohler et al. 2002; Keysers et al. 2003)]. Taken together,
it has been suggested that the activity of mirror neurons
holds information regarding action goals even in the
absence of complete sensory information describing it.
Therefor it seems that the activity of mirror neurons in
fronto-parietal circuits is loosely tied to the physical attri-
butes of sensory input and more sensitive to the goals of
perceived actions. Although understanding of goals
requires conscious perception of actions, it is not yet
known to what extent activity in the mirror system
depends on the degree of conscious perception of an
action. Behavioral studies in humans indeed suggest that
an unconscious process of imitation takes place during
observation of actions performed by others, resulting in
an increased tendency to perform similar actions (e.g.,
social contagion/the chameleon effect, Chartrand and
Bargh 1999). Such implicit imitation could be the result
of mirror neuron activity (Hogeveen and Obhi 2012;
Cross and Iacoboni 2014).
At the physiological level, suppression of oscillatory
activity within the mu (813 Hz) and beta (1525 Hz)
frequency bands over sensory motor regions has been
associated with action execution. Similar suppression has
been reported also during action observation and thus
taken as an index to infer mirror neuron activity (Cochin
et al. 1998; Hari et al. 1998; Perry and Bentin 2009; Arn-
stein et al. 2011; Fren-kel-Toledo et al. 2013; for review
see Pineda 2005). In agreement with previous literature,
we used these indices to probe the activity of the mirror
neuron system and examine the level of mu and beta sup-
pression with respect to the level of conscious action per-
ception.
Methods
Participants
Nineteen healthy, right-handed adults (7 males) ranging
from the ages of 1933 participated in this study
(Mean =24.58, SD =2.98). All the subjects were right
handed, and had normal or corrected to normal vision.
Participants were recruited from the general population
of students at Tel Aviv University and were compensated
for their participation with either course credit or pay-
ment. Prior to the experiment, all participants provided
written informed consent to participate. The study was
approved, and conformed to the guidelines set by the Tel
Aviv University Ethical committee.
Stimuli
We modified the Continuous Flash Suppression (CFS)
paradigm (Tsuchiya and Koch 2005) to render action
videos (rather than static images) invisible to conscious
perception (For experimental design, see Fig. 1). The CFS
procedure allows masking from visual awareness an
otherwise visible stimulus presented to one eye, by simul-
taneously presenting strong dynamic noise to the opposite
eye. Target and masking stimuli were presented at the
center of a 3D monitor (Samsung led s23a950d, 120 Hz
refresh rate) at 17 cm
2
size and approximately 70 cm
from the participants’ eyes. Active shutter glasses that
were synchronized to the monitor enabled exclusive pre-
sentation of odd frames only to one eye and even frames
to the other eye. Since target and mask video frames were
presented in alternate sequence mode (i.e., one frame
from each video in turn), odd frames (corresponding to
the mask stimulus) were presented to one eye and the
even frames (corresponding to the target stimulus) were
presented to the other eye. The CFS display consisted of
one of three grayscale target videos of different hand
movements and one of three different masking videos of
colored Mondrian patterns. During each trial one eye was
presented with 3 sec masking video (180 mask frames)
and the other eye was presented with a black screen for
1 sec (60 frames) followed by 2 sec of the target video
(another 120 target frames). The first second of each CFS
display in each trial was used as baseline for the analysis.
Task
Each trial started with the presentation of a fixation point
(“+”) that lasted 2.5 sec followed by the 3 sec of CFS dis-
play. At the end of each trial participants reported their
level of conscious perception. First, they were asked to
report which of the three actions was presented, or guess
in case they did not consciously perceived it. The partici-
pants reported their perception level by two means. First,
by pressing one of three buttons corresponding to repre-
sentative frames taken from the target action video pre-
sented on the screen. The mapping between buttons and
action video frames was randomized across trials in order
to avoid motor preparation which has been shown to
result in mu and beta suppression (Pfurtscheller et al.
Brain and Behavior, doi: 10.1002/brb3.494 (2 of 11) ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
Action perception level and EEG power S. Simon & R. Mukamel
1996; Ohara et al. 2000; Rektor et al. 2006). Second, the
participants reported their confidence level, namely to
what extent they are confident in their report, on a scale
from 1 to 4. Participants were asked to report “4” in case
they could perceived a sequence of dynamic movement
and were sure which action out of the three was dis-
played. A report of “1” in confidence level corresponded
to cases in which they did not perceive the movement at
all and were forced to guess which action was displayed.
In case they could perceive the action based on a single
frame or a flash of an image they were asked to report an
intermediate level (“2” or “3”) of confidence.
Procedure
The experiment included four blocks, each consisted of
75 trials. For each participant we first ran a behavioral
pretest to set the level of perception to be as close to
50%. In the behavioral pretest, we presented each of the
three hand movement trials five times at six different
levels of brightness (ranging from 35 to 220 in grayscale).
The optimal brightness chosen for the main experiment
was the brightness that generated the most balanced dis-
tribution across confidence levels with at least three trials
with confidence level 1 and confidence level 4 respec-
tively. Subjects who did not meet these criteria in any
brightness level were excluded from participating in the
experiment.
Data acquisition
We used a Biosemi Active Two EEG recording system
(Biosemi B. V., Amsterdam, the Netherlands). Data were
recorded from 64 scalp-electrodes at locations of the
extended 1020 system, as well as from two electrodes
placed on the left and right mastoids. The horizontal elec-
tro-oculogram (EOG) was recorded from electrodes
placed 1 cm to the left and right of the eye to detect hori-
zontal eye movement, and the vertical EOG was recorded
from an electrode beneath the left eye to detect blinks
and vertical eye movements. The single-ended voltage was
recorded between each electrode site and a common
mode sense electrode (CMS/DRL). Data were sampled
and digitized at 256 Hz.
Data analysis
We focused on the modulations of mu (813 Hz) and
beta (1525 Hz) rhythms measured over the sensorimotor
cortex. Particularly, mu suppression in the range 810 Hz
was found to be more suppressed during action observa-
tion than action execution (Frenkel-Toledo et al. 2013).
Therefore, mu suppression indices were computed sepa-
rately for the lower mu frequency range (810 Hz) and
the higher mu frequency range (1113 Hz).
Preprocessing
Offline signal processing and analysis was performed
using EEGLAB Toolbox: RRID:SCR_007292 (Delorme
and Makeig, 2004) version 13.0.1 and custom MATLAB
scripts: RRID:SCR_001622. All EEG signals were refer-
enced offline to the average of the left and right mastoids
and bandpass filtered between 0.5 and 40 Hz. The contin-
uous data were segmented into epochs from 1000 to
+2000 ms relative to onset of the target stimuli. EEG
Figure 1. Experimental Design. During each trial two separate video clips were presented in an interleaved fashion such that odd frames
(corresponding with clip 1) were presented to one eye, and even frames (corresponding with clip 2) were presented to the other eye. Clip 1
consisted of 3 sec masking video, whereas clip 2 consisted of a black screen for 1 sec followed by 2 sec of a target video. The first second of
each trial was used as baseline for the analysis. At the end of each trial, participants reported which action was presented and their confidence
level on a scale from 1 to 4.
ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. Brain and Behavior, doi: 10.1002/brb3.494 (3 of 11)
S. Simon & R. Mukamel Action perception level and EEG power
deflections resulting from eye movements and blinks were
corrected using an ICA procedure (Jung et al. 2000).
Epochs with artifacts exceeding 100 lV amplitude in
the relevant electrodes were rejected. Trials were classified
to conditions based on the participants’ accuracy and
their reports of confidence level.
Event-related spectral perturbations
The integrated power in the 813 Hz and 1525 Hz
frequency ranges was computed using wavelet analysis.
For each trial in each subject, we computed the loga-
rithm of the power (from 500 to 2000 ms post target
stimulus) relative to power during baseline (from 500
to 0 ms pre target stimulus). The suppression indices
for each condition were then calculated by averaging
across subjects the single-trial log ratios values from
equal number of trials for each condition. A negative
log ratio indicates a suppression in EEG oscillations
amplitude relative to baseline, whereas positive log ratio
indicates enhancement. Suppression indices were com-
puted at two central sites, C3 and C4, which best
reflect changes in mu and beta rhythms (Pineda 2005).
As control, these measures were also computed at two
occipital sites, O1 and O2, where alpha (813 Hz)
rhythms are strongest. Suppression of occipital alpha is
induced during perceptual events (Pfurtscheller et al.
1994; Krause et al. 1996) and increased demands of
attention (Klimesch 1996; Thut et al. 2006; Palva and
Palva 2007; Sauseng and Klimesch 2008). Since the per-
ception of our target may capture participants’ attention
more than the Mondrian patterns (in the case of non-
perceived trials), both occipital alpha and sensorimotor
mu are reported.
Results
Two subjects had too few nonperceived trials (<25 trials)
and were therefore excluded from further analysis.
Behavior
At the behavioral level, participants (N=17) reported
they fully perceived the action (“4” in confidence level) in
40.2% of the trials (range: 1072%), out of which 97.8%
were indeed correctly reported (range: 92.3100%). Par-
ticipants reported they did not perceive the action at all
(“1” in confidence level) in 36.1% of the trials (range:
14.683%), out of which 71.2% were indeed incorrectly
reported (range: 62.7186.75%). Intermediate levels of
perception (“2” and “3” in confidence level), were
reported in 14.4% and 9.4% of the trials, respectively
(62.7% trials with confidence level “2” and 86.55% with
confidence level “3” were correctly reported). These
results imply that reports of confidence level correspond
with performance accuracy (Fig. 2).
Event-related spectral perturbations
We first analyzed mu and beta rhythm power changes for
trials in which participants correctly reported the actions
with the highest confidence level (“Perceived” trials) and
trials with incorrect responses with the lowest confidence
level (“Nonperceived” trials).
We analyzed the differences in suppression indices
using repeated-measures analysis of variance (ANOVA)
with the factors of Condition (“Perceived”, “Nonper-
ceived”), Channel (“C3”, “C4”, “O1”, “O2”), and Band
(“Low Mu”, “High Mu”, and “Beta”). Pvalues for effects
that introduced violation of sphericity were corrected
using lower-bound epsilon values (Geisser and Green-
house 1958). ANOVA showed significant main effects for
all factors: Condition (F(1,16) =10.03, P<0.01), Chan-
nel (F(1,16) =7.23, P<0.01), and Band (F(1,16) =5.00,
P<0.05). These main effects were qualified by third
order interaction of Condition 9Channel 9Band (F
(1,16) =9.041, P<0.01). This interaction was further
examined with planned comparisons using one-tailed
pairwise t-tests. Over both the left and right sensory
motor cortices (channels C3 and C4), the oscillation
power in the Beta range (1525 Hz) was significantly
lower in the Perceived versus Nonperceived trials (“Per-
ceived” “Nonperceived” Mean difference (Md) Stan-
dard Error of the Mean (SEM) =0.35 0.07 dB, t
(16) =2.47, P<0.05 in C3 and 0.33 0.02 dB, t
(16) =1.97, P<0.05 in C4). Oscillation power in the
low mu range (810 Hz) was significantly lower in the
Perceived versus Nonperceived trials, but only over the
0
20
40
60
80
100
1234
% of Trials
Confidence Level
Correct Incorrect
Figure 2. Behavioral Results. Correct reports corresponded to higher
confidence levels, whereas incorrect reports corresponded to lower
confidence levels (Error bars represent Standard Deviation).
Brain and Behavior, doi: 10.1002/brb3.494 (4 of 11) ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
Action perception level and EEG power S. Simon & R. Mukamel
left sensorimotor site (Md SEM =0.25 0.03 dB, t
(16) =1.92, P<0.05 in C3 and 0.09 0.03 dB, t
(16) =0.55, P=0.31 in C4). In the higher mu frequency
range (1113 Hz), the oscillation power was not signifi-
cantly different across trial types (Md
SEM =0.06 0.02 dB, t(16) =0.44, P=0.33 in C3
and 0.22 0.04 dB, t(16) =1.34, P=0.1 in C4)
(Fig. 3). At the left and right occipital sites, oscillation
power in the beta frequency range was not significantly
different across perception levels (Md SEM =
0.04 0.02 dB, t(16) =0.35, P=0.46 in O1 and
0.01 0.02 dB, t(16) =1.13, P=0.44 in O2; one-tailed,
paired t-test). The difference between perception levels in
the low alpha range (810 Hz) was found significant in
(A)
(B)
Figure 3. Mu and Beta suppression in Central sites (N=17). Mu and Beta oscillation power for the “Perceived” and “Nonperceived” trials over
the left (“C3”) and right (“C4”) sensorimotor cortices in the range of beta (1525 Hz), high mu (1113 Hz), and low mu (810 Hz). (A) Event-
Related Spectral Perturbations representing changes in oscillation power locked to target display (time 0 ms) relative to baseline (500 to 0 ms).
(B) Stronger suppression for perceptually perceived trials was found in bilateral beta and left low mu frequency ranges. Additionally, power in the
beta range in both hemispheres was significantly suppressed in the Nonperceived trials relative to baseline (*P<0.05 corrected, Error bars
represent Standard Error).
ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. Brain and Behavior, doi: 10.1002/brb3.494 (5 of 11)
S. Simon & R. Mukamel Action perception level and EEG power
the left occipital site and marginally significant at the right
occipital site (Md SEM =0.34 10
3
dB, t
(16) =1.86, P<0.05 in O1 and 0.26 0.07 dB, t
(16) =1.36, P=0.09 in O2) (Fig. 4). In the higher alpha
frequency range (1113 Hz), the oscillation power was not
significantly different across the two trial types (Fig. 4).
We further inspected each channel and band suppres-
sion indices in the “Nonperceived” trials relative to base-
line using one-tailed pairwise t-tests (Bonferroni corrected
for the four channels in each frequency band). Only sup-
pression indices in the beta range were significant
(M SEM =0.42 0.08 dB, t(16) =5.05, P<0.01 in
(A)
(B)
Figure 4. Alpha and Beta suppression in Occipital sites (N=17). Alpha and Beta oscillation power for the “Perceived” and “Nonperceived” trials
over the left (“O1”) and right (“O2”) visual cortices in the range of beta (1525 Hz), high alpha (1113 Hz), and low alpha (810 Hz). (A) Event-
Related Spectral Perturbations representing changes in oscillation power locked to target display (time 0 ms) relative to baseline (500 to 0 ms).
(B) Stronger suppression for the perceptually perceived trials was found only in the low alpha frequency range over O1 (and marginally significant
in O2, see text). Power in the beta frequency was significantly suppressed in the nonperceived trials relative to baseline (*P<0.05 corrected,
Error bars represent Standard Error).
Brain and Behavior, doi: 10.1002/brb3.494 (6 of 11) ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
Action perception level and EEG power S. Simon & R. Mukamel
C3, 0.32 0.05 dB, t(16) =3.11, P<0.01 in C4,
0.35 0.03 dB, t(16) =2.03, P<0.01 in O1, and
0.23 0.04 dB, t(16) =2.87, P<0.01 in O2; one-
tailed paired t-test) (Figs 3B and 4B).
We also inspected to what degree the level of percep-
tion is correlated with the level of low mu and beta sup-
pression. To that end, we computed the mu and beta
suppression indices also for the partial perception trials -
all the trials in which the subjects reported partial (“2” or
“3”) confidence level. Since partial levels of perception
were reported in considerably fewer number of trials, only
11 subjects that passed the criterion of 25 trials per per-
ception level (“full”, “partial”, and “none” perception
levels) were included in this analysis. We observed a mar-
ginally significant within effect linear trend in the beta
range over the left and the right sensory motor regions (F
(1,10) =3.98, P=0.07 in C3 and F(1,10) =3.55,
P=0.09 in C4) which was significant when each subject’s
suppression index was averaged across C3 and C4 (F(1,
10) =5.42, P<0.05). In the low mu range, we found a
marginally significant linear trend but only over the left
sensorimotor region (F(1,10) =4.14, P=0.08 in C3 and
F(1,10) =0.37, P=0.84 in C4). Linear trends in the
occipital sites were far from reaching significance (F
(1,10) =0.06, P=0.8 in O1 and F(1,10) =0.64, P=0.43
in O2, in the beta range and F(1,10) =1.10, P=0.31 in
O1 and F(1,10) =1.62, P=0.23 in O2 in the low mu
range) (Fig. 5).
Discussion
In this study, we investigated whether and to what degree
activity in the mirror neuron system depends on con-
scious perception of actions. To this end, we rendered
hand movement videos invisible to conscious perception
and measured the magnitude of corresponding mirror
activity via the modulation of EEG mu and beta oscilla-
tion power over the sensorimotor cortices. We found
variations between the modulations of the two frequency
bands. Oscillation power in the range of beta over both
the right and left central sites, was significantly reduced
during observation of conscious relative to unconscious
perception of actions, as well as during unconscious
action perception relative to baseline. Oscillation power
in the range of mu, however, was significantly reduced
only in the low range (810 Hz) and only in left central
site, during conscious perception relative to unconscious
perception. Relative to baseline, the mu oscillation power
was not significantly suppressed.
Stronger mu and beta suppression over the bilateral
sensorimotor cortices in conscious relative to unconscious
perception have been reported in sensory modalities
Figure 5. Power suppression in low Mu\Alpha and Beta (N=11) and perception level. Low mu (8-10 Hz) and beta (15-25 Hz) oscillation power
for the “Full”, “Partial”, and “None” perception level trials over the left (in dark) and right (in light) sensorimotor and occipital cortices. The
graphs represent the changes in averaged suppression index across subjects at each of the three perception levels. A significant linear trend was
found only for the averaged suppression index in the central sites at the beta range (*P<0.05, Error bars represent Standard Error).
ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. Brain and Behavior, doi: 10.1002/brb3.494 (7 of 11)
S. Simon & R. Mukamel Action perception level and EEG power
including the tactile and auditory domains. In a MEG
study, mu and beta suppression over the bilateral primary
somatosensory cortices were more suppressed between
perceived versus not perceived tactile stimulation, and
nonperceived tactile stimulation was significantly sup-
pressed relative to baseline (Palva et al. 2005). Similarly,
EEG oscillations in the mid-frequency range (1220 Hz),
have been reported to reflect auditory illusion intensity,
with stronger power reductions corresponding with stron-
ger percepts (Leske et al. 2013).
In this study, we observed lateralized effects only in the
low mu frequency band. Mu oscillation power was signifi-
cantly more reduced for perceived versus not perceived
actions only in the low range (810 Hz) and over the left
central site. This lateralization is unlikely to reflect the
fact that subjects used their right hand to report their
subjective perception since subjects had to prepare equally
to report perceived and nonperceived trials. Our result is
in agreement with previous findings that addressed the
mirror neuron system showing that observation of a mov-
ing hand elicits stronger mu suppression (Perry and Ben-
tin 2009; Perry et al. 2011) as well as stronger fMRI
signal response (Shmuelof and Zohary 2005; Lorey et al.
2013) in the hemisphere contralateral to the observed
hand. Our stimuli consisted of right hand movements,
compatible with a stronger effect over the left, contralat-
eral hemisphere in the consciously perceived trials.
Our finding of significant suppression relative to base-
line only in central beta during the “Nonperceived” trials,
point to a functional dissociation between mu and beta
with respect to conscious perception. Differences in oscil-
lation power levels between these frequency bands during
action observation were reported in other dimensions.
For example, Avanzini and colleagues (Avanzini et al.
2012) demonstrated that only central beta oscillation
power follows the temporal envelop of movement dynam-
ics. This suggests the processing and representation of
specific action kinematic aspects is carried by the beta
rhythm. Other studies conducted by Hari and colleges
with MEG add support to this assertion, demonstrating
that the sources of beta and mu rhythms are different, as
beta originate predominantly in the precentral primary
motor cortex, whereas mu rhythms originate in the pri-
mary sensorimotor cortex (Hari et al. 1997; Hari 2006).
Our ability to claim that our results are specific to the
mirror system activity is limited, as we did not examine
suppression characteristics for nonaction visual stimuli.
Nonetheless, we believe the current results are unlikely to
be accounted for by general nonspecific response to visual
stimuli. Studies that compared EEG responses to nonac-
tion (e.g., words or symbols) perceived versus identical
unperceived visual stimuli, report occipital to parietal
power suppression in beta (Minami et al. 2014;
Kloosterman et al. 2015) and alpha (Babiloni et al. 2006;
Gaillard et al. 2009; Bazanova and Vernon 2014). Here
we report functional differences between perceived and
nonperceived action stimuli in central sites but not in
occipital sites. Additionally, the differences and the linear
trend we measured between perception levels at central
sites in the beta range, were not observed at the occipital
sites. Finally, the lateralization we measured between the
left and right central sites in the low mu range, were not
observed at occipital sites. Interestingly, an EEG study
that examined the neural activity during conscious versus
unconscious processing of tools, reported stronger mu
(813 Hz) suppression over the left centro-parietal
regions for visible versus invisible tools conditions, and
significant mu suppression for the invisible tool condition
relative to baseline. Stronger suppression in beta was
obtained for visible versus invisible tools as well (Suzuki
et al. 2014). Passive observation of manipulable objects
that afford possible actions, has been shown to elicit simi-
lar neural responses to passive observation of others’
actions (i.e., Canonical Neurons, Creem-Regehr and Lee
2005; Caggiano et al. 2009; Cisek and Kalaska 2010;
Proverbio et al. 2011; Proverbio 2012). Taken together,
the central mu and beta modulations we found for per-
ceived versus nonperceived actions seem more likely to be
specific to observed actions.
Our interpretation that mirror system activity depends
on the level of action perception is compatible with EEG
and MEG studies showing weaker suppression to visible
but unattended actions. In these studies, subjects were
presented with actions while they performed an orthogo-
nal task. Attentional modulations were correlated with
modulations both in mu (Perry and Bentin 2010; Schuch
et al. 2010) and beta (Muthukumaraswamy and Singh
2008) oscillation power.
This study consisted of relatively limited number of tri-
als as trial type depended on subjective perception, there-
fore single-trial classification of perception level based on
oscillatory power suppression was not feasible. Future
studies using larger number of trials should address this
issue and examine whether perception can be classified
not only based on power suppression in response to the
stimulus, but also predicted based on spontaneous pres-
timulus activity (i.e., oscillatory power prior to trial
onset).
Conclusion
Our data demonstrate that the degree of mirror neurons
activity depends on the level of action perception, which
is in line with theories associating the mirror system func-
tion with action understanding and understanding inten-
tions of others. Yet, our data also imply that the mirror
Brain and Behavior, doi: 10.1002/brb3.494 (8 of 11) ª2016 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
Action perception level and EEG power S. Simon & R. Mukamel
neuron system responds significantly to actions that are
not consciously perceived, which indicates that such
actions are also being processed to some degree. The
behavioral effect of implicit imitation (e.g., the chameleon
effect) is in line with such physiological responses.
Acknowledgments
This study was supported by the I-CORE Program of the
Planning and Budgeting Committee and The Israel
Science Foundation (grant No. 51/11), The Israel Science
Foundation (grants No. 1771/13 and 2043/13), and
Human Frontiers Science Project (HFSP) Career Develop-
ment Award (CDA00078/2011-C) (R. Mukamel); The
Yosef Sagol Scholarship for Neuroscience Research and
the Sagol School of Neuroscience Fellowship (S. Simon).
The funders had no role in study design, data collection
and analysis, decision to publish, or preparation of the
manuscript. The authors thank Michal Geron for help
with data acquisition, Ori Ossmy, Roee Gilron, Daniel
Reznik, Matan Mazor, and Shlomit Yuval-Greenberg for
their fruitful comments on the manuscript.
Conflict of interest
None declared.
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S. Simon & R. Mukamel Action perception level and EEG power
... We recorded TEPs from the right M1 to assess cortical connectivity patterns. We focused on the source-level functional connectivity profile of M1 in typical and newly acquired motor resonance conditions across alpha (8-12 Hz) and beta (13-30 Hz) frequency bands, which are known to be crucial for the sensorimotor system activity during action observation (Babiloni et al., 2016;Muthukumaraswamy and Johnson, 2004;Qin et al., 2023;Simon and Mukamel, 2016). Simultaneously, we recorded MEPs from two muscles of the left hand (i.e., first dorsal interosseus -FDIand abductor digiti minimi -ADM) to investigate corticospinal motor resonance and control for the protocol's effectiveness. ...
... Subsequently, the debiased weighted Phase Lag Index -wPLI (Vinck et al., 2011) was calculated to assess connectivity between the right M1 and other brain parcels within the alpha (8-12 Hz) and beta (13-30 Hz) frequency bands for each task's condition. We decided to focus our investigation on these two frequency bands, considering their prominent role in action observation and AON functioning (Babiloni et al., 2016;Muthukumaraswamy and Johnson, 2004;Qin et al., 2023;Simon and Mukamel, 2016). ...
... M1 interregional communication in alpha and beta bands could reflect dissociable aspects of human mirroring phenomena, displaying how typical motor resonance is implemented within the motor network and how this mechanism's plasticity unfolds during the acquisition of a new visuomotor association. This evidence is in line with previous studies highlighting the relevance of alpha and beta rhythms during action observation (Babiloni et al., 2016;Muthukumaraswamy and Johnson, 2004;Qin et al., 2023;Simon and Mukamel, 2016), although most of these investigations primarily focused on regional oscillatory activity instead of addressing oscillatory networks, as in the present work. ...
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Motor resonance – the facilitation of corticospinal excitability during action observation – is considered a proxy of Action Observation Network (AON) recruitment in humans, with profound implications for social cognition and action understanding. Despite extensive research, the neural underpinnings supporting motor resonance emergence and rewriting remain unexplored. In this study, we investigated the role of sensorimotor associative learning in neural mechanisms underlying the motor resonance phenomenon. To this aim, we applied cross-systems paired associative stimulation (PAS) to induce novel visuomotor associations in the human brain. This protocol, which repeatedly pairs transcranial magnetic stimulation (TMS) pulses over the primary motor cortex (M1) with visual stimuli of actions, drives the emergence of an atypical, PAS-conditioned motor resonance response. Using TMS and electroencephalography (EEG) co-registration during action observation, we tracked the M1 functional connectivity profile during this process to map the inter-areal connectivity profiles associated with typical and PAS-induced motor resonance phenomena. Besides confirming, at the corticospinal level, the emergence of newly acquired motor resonance responses at the cost of typical ones after PAS administration, our results reveal dissociable aspects of motor resonance in M1 interregional communication. On the one side, typical motor resonance effects acquired through the lifespan are associated with prominent M1 alpha-band and reduced beta-band connectivity, which might facilitate the corticospinal output while integrating visuomotor information. Conversely, the atypical PAS-induced motor resonance is linked to M1 beta-band cortical connectivity modulations, only partially overlapping with interregional communication patterns related to the typical mirroring responses. This evidence suggests that beta-phase synchronization may be the critical mechanism supporting the formation of motor resonance by coordinating the activity of motor regions during action observation, which also involves alpha-band top-down control of frontal areas. These findings provide new insights into the neural dynamics underlying (typical and newly acquired) motor resonance, highlighting the role of large-scale interregional communication in sensorimotor associative learning within the AON.
... We recorded TEPs from the right M1 during this task to assess cortical connectivity patterns. We focused on the source-level functional connectivity profile of M1 in typical and newly acquired motor resonance conditions across alpha (8-12 Hz) and beta (13-30 Hz) frequency bands, which are known to be crucial for the sensorimotor system activity during action observation (e.g., Babiloni et al., 2016;Muthukumaraswamy & Johnson, 2004;Qin et al., 2023;Simon & Mukamel, 2016). Simultaneously, we recorded MEPs from two muscles of the left hand (i.e., first dorsal interosseus -FDI -and abductor digiti minimi -ADM) to investigate motor resonance at the corticospinal level and control for the protocol's effectiveness. ...
... Subsequently, the debiased weighted Phase Lag Index (wPLI, Vinck et al., 2011) was calculated to assess connectivity between the right M1 and other brain parcels within the alpha (8-12 Hz) and beta (13-30 Hz) frequency bands for each task's condition. We decided to focus our investigation on these two frequency bands, considering their prominent role in action observation and AON functioning (Babiloni et al., 2016;Muthukumaraswamy & Johnson, 2004;Qin et al., 2023;Simon & Mukamel, 2016). ...
... M1 interregional communication in alpha and beta bands could reflect dissociable aspects of human mirroring phenomena, displaying how typical motor resonance is implemented within the motor network and how this mechanism's plasticity unfolds during the acquisition of a new visuomotor association. This evidence is in line with previous studies highlighting the relevance of alpha and beta rhythms during action observation (Babiloni et al., 2016;Muthukumaraswamy & Johnson, 2004;Qin et al., 2023;Simon & Mukamel, 2016), although most of these investigations primarily focused on regional oscillatory activity instead of addressing oscillatory networks, as in the present work. ...
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Motor resonance – the activation of the observer’s motor system when viewing others’ actions – grounds the intertwined nature of action perception and execution, with profound implications for social cognition and action understanding. Despite extensive research, the neural underpinnings supporting motor resonance emergence and rewriting remain unexplored. In this study, we investigated the role of sensorimotor associative learning in motor resonance neural mechanisms. To this aim, we applied cross-systems paired associative stimulation (PAS) to induce novel visuomotor associations in the human brain. This protocol, which repeatedly pairs transcranial magnetic stimulation (TMS) pulses over the primary motor cortex (M1) with visual stimuli of actions, drives the emergence of an atypical, PAS-conditioned motor resonance response. Using TMS and electroencephalography (EEG) co-registration during action observation, we tracked the M1 functional connectivity profile during this process to map the inter-areal connectivity profiles associated with typical and PAS-induced motor resonance phenomena. Besides confirming, at the corticospinal level, the emergence of newly acquired motor resonance responses at the cost of typical ones after PAS administration, our results reveal dissociable aspects of motor resonance in M1 interregional communication. On the one side, typical motor resonance effects acquired through the lifespan are associated with prominent M1 alpha-band and reduced beta-band connectivity, which might facilitate the corticospinal output while integrating visuomotor information. Conversely, the atypical PAS-induced motor resonance is linked to M1 beta-band cortical connectivity modulations, only partially overlapping with interregional communication patterns related to the typical mirroring responses. This evidence suggests that beta-phase synchronization may be the critical mechanism supporting the formation of motor resonance by coordinating the activity of motor regions during action observation, which also involves alpha-band top-down control of frontal areas. These findings provide new insights into the neural dynamics underlying (typical and newly acquired) motor resonance, highlighting the role of large-scale interregional communication in sensorimotor associative learning within the action observation network.
... Typical results of passive observations of movements and experiments using imitations identifi ed many cortical areas displaying greater al., 2016], tennis players [Denis et al., 2017], cosmonauts [Cebolla et al., 2016], and pilots [Sestito et al., 2018]. Among the experimental paradigms used, the most common hav eused videos [Angelini et al., 2018;Isoda et al., 2016;Kim and Kim, 2016;Shibuya et al., 2019;Simon and Mukamel, 2016;Denis et al., 2017;Heimann et al., 2017;Riečansky et al., 2020;Pomiechowska and Csibra, 2017;Yin et al., 2017;Gutsell et al., 2020], images [Sestito et al., 2018], and real objects [Kompatsiari et al., 2021]; performance of certain actions [Lin et al., 2020;Park et al., 2018;Cuellar et al., 2016;Rimbert et al., 2018;Kooiman et al., 2020;Wen et al., 2017;Pereira et al., 2018;Cebolla et al., 2016;Peled-Avron et al., 2018;Fitzpatrick et al., 2019;Nishimura et al., 2018], as well as a combination of performance and observation of movements [Coll et al., 2017;Aridan et al., 2018;Krol et al., 2020;Malcolm et al., 2018]. In addition, methods which have been used to modulate the mu rhythm include tactile stimulation [Coll et al., 2017;Shibuya et Ensenberg et al., 2017]. ...
... Most studies do not mention the MNS or only mention it in passing; many use it only for theoretical grounding, though some authors directly link results obtained on mu-rhythm suppression with the mirror neuron system. For example, it was reported that auditory stimuli can activate the human mirror neuron system when sounds are associated with actions [Wu et al., 2016]; activation of the MNS was linked with the predictability of the action [Krol et al., 2020]; a short period of physical preparation increased activation of the mirror system on observation of actions [Brunsdon et al., 2020]; mirror system reaction intensity during observation of actions decreased with the level of consciousness of perception by the observer [Simon and Mukamel, 2016]. ...
... A decrease in mu-rhythm power during presentation of the swing of a prosthetic leg compared with walking without a prosthesis was found, which may point to increased motor planning and sensorimotor integration [Kooiman et al., 2020]. Also found were relationships between the extent of mu-rhythm desynchronization and the rate of passive movement [Iwane et al., 2019], the predictability of the performed and observed action [Krol et al., 2020], the observer's level of awareness of perception [Simon and Mukamel, 2016], the visual features of the actions (for example, different visual perspectives) [Angelini et al., 2018;Heimann et al., 2019;Heimann et al., 2017;Riečansky et al., 2020] and objects (for example, a "confl ict of affordances" decreased mu-rhythm desynchronization [Wamain et al., 2018] and the reality of objects increased desynchronization [Marini et al., 2019]) observed, and the subjects' experience with the experimental tasks assigned to them [Wu et al., 2016;Sestito et al., 2018;Denis et al., 2017]. A higher level of desynchronization of the α component of the mu rhythm was seen in conditions of performance of actions with the eyes closed as compared with open; it should be noted that these differences were not seen for the β component of the mu rhythm [Rimbert et al., 2018]. ...
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The mu rhythm is of interest in research into a wide range of processes, from motor functions to language processes and emotions. This rhythm includes at least two nonharmonic components in the α (8–13 Hz) and β (15–25 Hz) frequency ranges, with different functional roles, indicating the need for them to be studied independently. Overlap with α activity requires the effects of changes in attention to be monitored, with consideration of electrical activity not confined to the central leads, and also the application of mathematical methods of discriminating the mu and α rhythms. Mu rhythm suppression has been proposed as an index of arousal for the mirror neuron system, which has provoked much discussion and many studies, including those linked with the potential mixing of mirror neuron system activity and attention system activity. This review addresses current research in the context of these three aspects and includes results from the authors’ own research.
... Barone and Rossiter 2021). Several studies have shown that the power in the beta range, particularly in the high-beta range from 20-30Hz, is modulated by action observation confirming that it may be important for feedback processes also during action observation (Babiloni et al. 2016;Moreno, de Vega, and León 2013;Muthukumaraswamy and Johnson 2004;Simon and Mukamel 2016). Here we found that observation of actions in predictable order caused higher high-beta power in, and higher high-beta coherence between, precentral and supramarginal cortices. ...
... These effects were observed in the high-beta range (above 20Hz), and not in the lower beta range (15-20Hz). The specific role of subbands in the beta range remains poorly understood, but a small number of studies point towards a particular relevance of high-beta for integration of motor signals (Mooshagian, Holmes, and Snyder 2021;Tia et al. 2017), with the high-beta range selectively altered during the observation of other people's actions (Simon and Mukamel 2016). ...
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Predictive coding as a theoretical framework that has received much attention in recent years is often used to explain the mechanisms underlying various cognitive functions, especially during motor observation when prediction of others' behavior is crucial for successful social interactions. The action observation network(AON) has been extensively studied and confirmed, but the interactions between the main regions of AON are still not well understood. Here we made use of the high spatial and temporal resolution of intracranial Electrocorticography (ECoG), to test the functions and interactions of the key nodes of AON including precentral, supramarginal and visual areas. We found more top-down beta oscillation from precentral to supramarginal during the observation of predictable actions while more bottom-up gamma oscillation from visual to supramarginal for unpredictable action s.These provide strong evidence to illustrate how our brain perceive and understand other people's actions in a predictive manner.
... The results revealed an increased beta suppression in the complex conditions. Beta suppression, often observed concurrently with mu rhythm suppression, is known to be associated with motor execution or observation [51,52,[65][66][67][68][69][70]. One characteristic that sets beta rhythms apart from mu rhythms within the alpha frequency band is the beta rebound, or a transient increase in the power of the beta frequency band after a motor action is completed [67,68,[71][72][73][74][75][76], which could potentially account for the observed discrepancy in beta suppression. ...
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This study investigates the influence of immersive media, particularly Virtual Reality (VR), on empathic responses, in comparison to traditional television (TV), using electroencephalography (EEG). We employed mu rhythm suppression as a measurable neural marker to gauge empathic engagement, as its increase generally signifies heightened empathic responses. Our findings exhibit a greater mu rhythm suppression in VR conditions compared to TV conditions, suggesting a potential enhancement in empathic responses with VR. Furthermore, our results revealed that the strength of empathic responses was not confined to specific actions depicted in the video clips, underscoring the possibility of broader implications. This research contributes to the ongoing discourse on the effects of different media environments on empathic engagement, particularly emphasizing the unique role of immersive technologies such as VR. It invites further investigation into how such technologies can shape and potentially enhance the empathic experience.
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We studied the reactivity features of the EEG mu rhythm amplitude in the individually determined frequency range, as well as the beta rhythm in the central, frontal and parietal EEG leads in children while performing tasks for instrumental, emotional and altruistic helping behavior. The study engaged 24 children aged 4 to 7 years. ANOVA showed a significant decrease of the mu rhythm amplitude in the central and parietal regions, which is supposed to be associated with the activation of the mirror system of the brain. When performing tasks for instrumental and altruistic helping behavior, there was an increase in the amplitude of the beta rhythm in the frontal, central, and parietal regions, which may be associated with children observing actions that are emotionally charged and cause empathy with a person in need of help. The more the beta rhythm increased, the sooner the children provided help, which can be explained by a greater degree of emotional involvement and activation of cognitive processes in children with high performance of prosocial behavior.
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Mirror neurons were discovered over twenty years ago in the ventral premotor region F5 of the macaque monkey. Since their discovery much has been written about these neurons, both in the scientific literature and in the popular press. They have been proposed to be the neuronal substrate underlying a vast array of different functions. Indeed so much has been written about mirror neurons that last year they were referred to, rightly or wrongly, as "The most hyped concept in neuroscience". Here we try to cut through some of this hyperbole and review what is currently known (and not known) about mirror neurons.
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The primate visual system is assumed to comprise two main pathways: a ventral pathway for shape and color perception and a dorsal pathway for spatial processing and visuomotor control. Previous studies consistently reported strong activation in the dorsal pathway (especially in the inferior parietal region) induced by manipulable object images such as tools. However, it is controversial whether the dorsal pathway retains this preferential activity to tool images under unconscious perception. In the present study, we used magnetoencephalography (MEG) and investigated spatio-temporal dynamics of neural responses to visible and invisible tool images. A presentation of visible tool images elicited a strong neural response over the parietal regions in the left hemisphere peaking at 400 msec. This response unique to the processing of tool information in the left parietal regions was still observed when conscious perception of tool images was inhibited by interocular suppression. Furthermore, analyses of neural oscillation signals revealed a suppression of μ rhythm (8–13 Hz), a neural index of movement execution or imagery, induced by both visible and invisible tools. Those results indicated that the neural circuit to process the tool information was preserved under unconscious perception, highlighting an implicit aspect of the dorsal pathway.
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Studies investigating the role of oscillatory activity in sensory perception are primarily conducted in the visual domain, while the contribution of oscillatory activity to auditory perception is heavily understudied. The objective of the present study was to investigate macroscopic (EEG) oscillatory brain response patterns that contribute to an auditory (Zwicker tone, ZT) illusion. Three different analysis approaches were chosen: 1) a parametric variation of the ZT illusion intensity via three different notch widths of the ZT-inducing noise; 2) contrasts of high-versus-low-intensity ZT illusion trials, excluding physical stimuli differences; 3) a representational similarity analysis to relate source activity patterns to loudness ratings. Depending on the analysis approach, levels of alpha to beta activity (10-20Hz) reflected illusion intensity, mainly defined by reduced power levels co-occurring with stronger percepts. Consistent across all analysis approaches, source level analysis implicated auditory cortices as main generators, providing evidence that the activity level in the alpha and beta range - at least in part - contributes to the strength of the illusory auditory percept. This study corroborates the notion that alpha to beta activity in the auditory cortex is linked to functionally similar states, as has been proposed for visual, somatosensory and motor regions. Furthermore, our study provides certain theoretical implications for pathological auditory conscious perception (tinnitus).