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Journal ArticleDOI

A causal role for primary motor cortex in perception of observed actions

01 Dec 2016-Journal of Cognitive Neuroscience (MIT Press)-Vol. 28, Iss: 12, pp 2021-2029
TL;DR: It is found that a disruption to M1 caused a reduction in an individual's sensitivity to interpret the kinematics of observed actions; the magnitude of suppression of motor excitability predicted this change in sensitivity.
Abstract: It has been proposed that motor system activity during action observation may be modulated by the kinematics of observed actions. One purpose of this activity during action observation may be to predict the visual consequence of another person's action based on their movement kinematics. Here, we tested the hypothesis that the primary motor cortex M1 may have a causal role in inferring information that is present in the kinematics of observed actions. Healthy participants completed an action perception task before and after applying continuous theta burst stimulation cTBS over left M1. A neurophysiological marker was used to quantify the extent of M1 disruption following cTBS and stratify our sample a priori to provide an internal control. We found that a disruption to M1 caused a reduction in an individual's sensitivity to interpret the kinematics of observed actions; the magnitude of suppression of motor excitability predicted this change in sensitivity.

Summary (3 min read)

INTRODUCTION

  • More recently, it has been suggested that, as well as a possible role in understanding the goal of an observed action, motor system activity during action observation might enable us to predict the kinematics of the observed action (Kilner, 2011; Kilner, Friston, & Frith, 2007).
  • A follow-on study (Macerollo, Bose, Ricciardi, Edwards, & Kilner, 2015) then compared healthy participants and movement disorder patients on the same task.
  • The aim of this study was to identify a causal role for M1 in this task by disrupting motor excitability using continuous theta burst stimulation (cTBS) over M1.
  • This enabled us, first, to a priori stratify their sample and, second, to correlate changes in CSE with their behavioral effect.

Participants

  • Participants had no history of neurological or psychiatric illness and had no medical reason to exclude them from having TMS.
  • All participants were right-handed and gave written informed consent before taking part.
  • This study was approved by the UCL research ethics committee, and all testing took place at the UCL Institute of Neurology, Queen’s Square.

Experimental Design

  • Each participant carried out an action observation behavioral task before and after the application of cTBS.
  • Singlepulse TMS was applied at varying time points throughout the experiment to provide a neurophysiological marker of the effect of cTBS on motor excitability.
  • A baseline measurement of CSE (20 MEPs) was taken before cTBS.
  • Following this, cTBS was applied over left M1 for 40 sec.
  • The participants then repeated the action observation task.

Behavioral Task

  • The task was programmed in MATLAB R2013b (The MathWorks, Natick, MA).
  • The participants’ task was to estimate 2022 Journal of Cognitive Neuroscience Volume 28, Number 12 how confident they thought the actor in the video was in each decision observed.
  • The gender of the actor and the choice location were equally balanced across the videos.
  • Videos were filmed with a bird’s eye view of the table so only the actors’ hands were visible.
  • All the videos were edited to ensure that the time from the start of the trial to picking up the marble remained the same, and therefore, any difference in RT before picking up the marble could not be used to deduce confidence; the only parameter available to measure confidence was movement speed.

MEP Analysis

  • Twenty MEPs were recorded at baseline and then at three time points following cTBS: (1) 10 min post-cTBS, (2) after Block 1 of the behavioral task, and (3) after Block 2 on completion of the behavioral task.
  • The peak-to-peak amplitude for each individual MEP was measured.
  • MEPs were logtransformed at the first level to normalize the data and then retransformed at the second level to maintain the original units for MEPs (mV).
  • The stability of MEP amplitudes across the three time points post-cTBS was determined using a one way repeated-measures ANOVA.

Behavioral Data Analysis

  • Confidence ratings were ordered based on ET from fastest to slowest and grouped into 10 bins per participant.
  • The distribution of mean differences was calculated, and the position of the true mean difference was determined to identify if the difference between the groups was significant.
  • The same analysis was conducted separately for the inhibition and facilitation groups using the pre- and post-cTBS data points to determine in each group if the change in gradient observed was significantly increased or decreased from zero.
  • Baseline sensitivity to observed movement speed before cTBS was also compared between groups using a two-tailed independent samples t test to ensure that there was no baseline difference between groups.

Effect of cTBS on CSE

  • MEPs recorded from the right FDI of each participant before and after cTBS provided a physiological measure of the efficacy of cTBS in disrupting the motor cortex.
  • The change in cortical excitability following cTBS was highly variable between participants and over time in an individual participant.
  • Representative MEP waveforms averaged over 20 MEPs or the grand average (3 × 20 MEPs) post-cTBS are shown from two individuals, which had differential responses to cTBS .

Effect of cTBS on Sensitivity to Action Kinematics

  • ETs from all the videos shown were divided into 10 bins, and the mean confidence rating across all participants for each bin was plotted before and after cTBS .
  • Participants were divided into an inhibition or facilitation group based on a positive or negative change in mean MEP amplitude following cTBS.
  • In addition, nonparametric permutation tests, which make no assumption as the distribution of the underlying data, were used to corroborate the above findings.
  • The permutation test revealed a significant group difference in change in gradient following cTBS between the inhibition and facilitation groups ( p = .018).

DISCUSSION

  • The authors found a significant difference in behavior between the two groups as well as a correlation between the magnitude of change in MEP amplitude and the 2026 Journal of Cognitive Neuroscience Volume 28, Number 12 degree of change in sensitivity to movement speed.
  • In addition, it is important to stress that in this study the MEPs were recorded when the participants were at rest and not when they were performing the observation task.
  • The vast majority of virtual lesion studies using repetitive stimulation typically include a sham control group to determine the specificity of the ROI in causally influencing any change in behavior recorded.
  • In the current study, a positive or negative change in MEP amplitude following cTBS was used to categorize participants into a facilitation or inhibition group.
  • The results of their study provide evidence that M1 is functionally employed during action observation and that activity in M1 during action observation is related to the kinematics of an observed action.

Acknowledgments

  • M. D. is funded by a BBSRC David Phillips fellowship (UK), the Royal Society (UK), and an FWO Odysseus project (Fonds Wetenschappelijk Onderzoek, Belgium).
  • Reprint requests should be sent to Clare E. Palmer, Sobell Department for Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London (UCL), 33 Queen Square, London, United Kingdom, WC1N 3BG, or via e-mail: clare.palmer.13@ucl.ac.uk.

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A Causal Role for Primary Motor Cortex in
Perception of Observed Actions
Clare E. Palmer
1
, Karen L. Bunday
1
, Marco Davare
1,2
, and James M. Kilner
1
Abstract
It has been proposed that motor system activity during
action observation may be modulated by the kinematics of
observed actions. One purpose of this activity during action ob-
servation may be to predict the visual consequence of another
persons action based on their movement kinematics. Here, we
tested the hypothesis that the primary motor cortex (M1) may
have a causal role in inferring information that is present in the
kinematics of observed actions. Healthy participants completed
an action perception task before and after applying continuous
theta burst stimulation (cTBS) over left M1. A neurophysiolog-
ical mar ker was used to quantif y the extent of M1 disruption
following cTBS and stratify our sample a priori to provide an
internal control. We found that a disruption to M1 caused a
reduction in an individuals sensitivity to interpret the kinemat-
ics of observed actions; the magnitude of suppression of motor
excitability predicted this change in sensitivity.
INTRODUCTION
It is now well established that the motor system is active
during both action execution and action observation
(Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; di Pellegrino,
Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). A portion of
the human ventral premotor cortex (PMv), often thought
to be analogous to F5 in the monkey, was the fir st area
in which mirror neurons (neurons that fire during action
execution and action observation) were identified; yet it
is now clear that populations of neurons throughout
the motor system, including PMd and M1, respond to
both action execution and observation (Kilner & Lemon,
2013). However, there is currently a lack of consensus as
to the functional role of this motor system activity during
action obse rvation. The majority of studies in this field
have tested the hypothesis that motor system activity in
some way facilitates the perception of the observed action
goal (Ferrari, Rozzi, & Fogassi, 2005; Gallese et al., 1996).
More recently, it has been suggested that, as well as a
possible r ole in understanding the goal of an observed
action, motor system activity during action observation
might enable us to predict the kinematics of the observed
action (Kilner, 2011; Kilner, Frist on, & Frith, 2007). Put
simply, our ability to infer the goal of an observed action
is dependent upon first inferring how that action is per-
formed. There is increasing behavioral evidence from
human studies that suggests that we are very sensitive
to changes in the kinematics of actions (Ansuini, Cavallo,
Bertone, & Becchio, 2014; Patel, Fleming, & Kilner, 2012;
Alaerts, Senot, et al., 2010; Becchio, Sartori, & Castiello,
2010; Ne al & Kilner, 2010; Sartori, Becchio, Bara, &
Castiello, 2009; Daprati, Wriessnegger, & Lacquaniti,
2006), and some evidence suggests that activity in the pri-
mary motor cortex (M1) is modulated by the kinematics of
an observed action (Press, Heyes, & Kilner, 2011; Alaerts,
Swinnen, & Wenderoth, 2010). This proposed role of the
motor system in being sensitive to the kinematics of an
observed action is consistent with how neuronal discharge
is modulated during action execution (Moran & Schwartz,
1999; Rizzolatti et al., 1988; Georgopoulos, Schwartz, &
Kettner, 1986). Indeed, the kinematics of executed actions
can be decoded from activity in both PMv and M1 (Bansal,
Truccolo, Vargas-Irwin, & Donoghue, 2012).
It has been shown that we are able to infer an individ-
uals subjective state based on the kinematics of their
moveme nts (Patel et al., 2012). In this study, observers
were able to correctly infer the confidence of participants
carrying out a forced-choice discrimination task using
only the observed movement kinematics, namely move-
ment speed. A follow-on study (Macerollo, Bose, Ricciardi,
Edwards, & Kilner, 2015) then compared healthy par-
ticipants and movement disorder patients on the same
task. They found that movement disorder patients were
significantly worse in their ability to infer confidence from
fast movement speeds that differed most from their own.
Although this result is consistent with a potential role of
action execution networks in inferring information from
the kinematics of observed actions, it is unclear whether
this behavioral effect is contingent upon activity in the
motor cortex.
The aim of this study was to identify a causal role for
M1 in this task by disrupting motor excitability using
continuous theta burst stimulation (cTBS) over M1. cTBS
1
UCL Institute of Neurology, London, UK,
2
KU Leuven
© 2016 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 28:12, pp. 20212029
doi:10.1162/jocn_a_01015

has been traditionally thought to have an inhibitory effect
on the output of the targeted area and is therefore used as
a virtual lesion technique; however, recent studies have
shown that this effect is very variable (Hamada, Murase,
Hasan, Balaratnam, & Rothwell, 2013; Huang, Edwards,
Rounis, Bhatia, & Rothwell, 2005). To quantify this inter-
subject variability, we recorded motor-evoked potentials
(MEPs) throughout the task as a neurophysiological
marker of the effect of cTBS on corticospinal excitability
(CSE). This enabled us, first, to a priori stratify our sample
and, second, to correlate changes in CSE with our behav-
ioral effect. We hyp othesized that a disruption to M1
would impair an individuals abil ity to infer subjective
information from the kinematics of observed actions.
METHODS
Participants
Twenty-four healthy participants (13 men, 11 women)
aged 2135 years old (mean ± SD: 24.91 ± 3.8 3) took
part in this study. Participa nts had no history of neuro-
logical or psychiatric illness and had no medical reason
to exclude them from having TMS. All participants were
right-handed and gave written informed consent before
taking part. This study was approved by the UCL research
ethics committee, and all testing took place at the UCL
Institute of Neurology, QueensSquare.
Experimental Design
Each participant carried out an action observation behav-
ioral task before and after the application of cTBS. Single-
pulse TMS was applied at varying time points throughout
the experiment to provide a neurophysiological marker
of the effect of cTBS on motor excitability. A baseline
measurement of CSE (20 MEPs) was taken before cTBS.
Following this, cTBS was applied over left M1 for 40 sec.
The participants then repeated the action observation
task. To measure the effect of cTBS on CSE, 20 MEPs
were measured at three time points following cTBS: 10 min
after repetitive stimulation, midway through the behav-
ioral task (approximately 25 min poststimulation), and on
completion of the behavioral task (approximately 40 min
poststimulation; see Figure 1A for protocol).
Behavioral Task
The task was programmed in MATLAB R2013b (The
MathWorks, Natick, MA). Participants watched 390 videos
divided into two blocks in a pseudorandomized order. In
each video, an actor picked up a marble from the center
of a table and moved it onto a marker on either the left or
the right. The videos were filmed during a previous study
in which these participants carried out a two alternate
forced-choice discrimination task and were asked to indi-
cate their decision by moving the marble (Patel et al.,
2012). In this study, the participants task was to estimate
Figure 1. Experimental procedure. (A) Timeline of experimental protocol. The action observation task (gray squares) was completed twice,
before and after cTBS. Blocks of 20 MEPs were recorded using single-pulse TMS at baseline and at three time points starting 10 min post-cTBS
(red circles). (B) Still frames of the action observation task. Participants (n = 24) watched videos in which an individual performed a two alternative
forced-choice discrimination task. The left and right sides were assigned to the two choices. The participants in the video had to move the marble
to either side to indicate their decision. White arrows indicate hand movement. Movement speed was calculated from the time the hand was
released from its starting point (Frame 2) to the time the marble was placed on the left or right of the screen (Frame 4). Observers were instructed
to rate the confidence of the participant making the decision in the video after each trial on a scale of 1100 from not confident to very confident
(Frame 5).
2022 Journal of Cognitive Neuroscience Volume 28, Number 12

how confident they thought the actor in the video was in
each decision observed. Participants were instructed to
rate the confidence of the actor by moving a cursor along
a0100 scale bar (Figure 1B). The gender of the actor and
the choice location were equally bala nced across the
videos. Videos were filmed with a birds eye view of the
table so only the actors hands were visible. All the videos
were edited to ensure that the time from the start of the
trial to picking up the marble remained the same, and
therefore, any difference in RT before picking up the mar-
ble could not be used to deduce confidence; the only pa-
rameter available to measure confidence was movement
speed. Execution time (ET) was used as a proxy for move-
ment speed and was calculated as the time from the mo-
ment the marble was removed from its original marker to
the time it was placed on one of the choice markers.
Catch trials in which the actor hesitated or dropped the
marble were removed post hoc. Each participant carried
out the task twice before and after cTBS.
Single-pulse TMS
EMG activity was recorded from the right first dorsal
interosseous (FDI) muscle using Ag/AgCl cup electrodes
in a bellytendon montage. The EMG signal was ampli-
fied 1000×, low-pass filtered at 3 Hz, sampled at 5 kHz,
and stored for offline analysis (CED 1401 with signal soft-
ware, version 5.10, Cambridge Electronic Design, Cambridge,
UK) A Magstim 200 stimulator (Magstim, Carmarthenshire,
UK) was used to deliver monopha sic TMS pulses to the
hand area of the left primary moto r cortex (M1). The
figure-of-eight coil (9 cm diameter) was held tangentially
to the head over the optimal hotspot for producing
MEPs. Resting and active motor thresholds (RMT, AMT)
were recorded for each participant. Motor threshold was
defined as the minimum intensity of the stimulator output,
which produced an MEP greater than 50 μV on 6 of 10 con-
secutive pulses. AMT was determined while participants
produced a steady isometric contraction against an inert
object to produce a constant EMG output at 10% of their
maximum voluntary contraction. The AMT was used to
determine the intensity of stimulator output for cTBS;
the Magstim Rapid2 (Magstim) was used to find the AMT.
Baseline measurements were taken at a stimulator out-
put intensity, which produced a mean MEP amplitude of
1mV.Thesameintensitywasusedthroughoutthe
experiment to record MEPs. RMT = 41.76 ± 7.43% of
maximum stimulator output (MSO; Magstim 200). AMT =
50.28 ± 7.44% of MSO (Mags tim Rapid2; AMT > RMT
due to different stimulators used). Baseline stimulator
intensity = 48.16 ± 9.10% of MSO (Magstim 200).
Continuous Theta Burst Stimulation
cTBS was delivered using a Magstim Rapid2 stimulator
(Magstim) as a sequence of 200 bursts at a rate of 5 Hz
(total duration 40 sec). Each burst consisted of three
stimuli given at 50 Hz. The stimulator output intensity
for cTBS was 80% of AMT (Huang et al., 2005).
MEP Analysis
Twenty MEPs were recorded at baseline and then at three
time points following cTBS: (1) 10 min post-cTBS, (2)
after Block 1 of the behavioral task, and (3) after Block
2 on completion of the behavioral task. The peak-to-peak
amplitude for each individual MEP was measured. MEPs
were excluded if there was EMG activity (>0.1 mV) 100 msec
before the TMS pulse was given (3.85% of total MEPs).
One participant was excluded because of high back-
ground EMG activity througho ut the baseline resulting
in significantly fewer MEPs being analyzed (one-sample
t test: t(23) = 55.75, p < .001; mean difference in
number of MEPs at baseline = 5.83). MEPs were log-
transformed at the f irst level to normalize the data and
then retransfor med at the second level to maintain the
original units for MEPs (mV). Magnitude of MEP sup-
pression was calculated as the difference between the aver-
age normalized MEP amplitude at baseline and the grand
average of normalized MEP amplitude at three time points
post-cTBS. MEP amplitude was stable across time points
poststimulation: A repeated-measures ANOVA revealed
no significant mai n effect of Time, and none of the pairwise
comparisons were significant ( p > .1). An inhibitory
response to cTBS was defined as a magnitude of MEP sup-
pression greater than 0 and a facilitatory response less than
0 (López-Alonso, Cheeran, Río-Rodríguez, & Fernández-
del-Olmo, 2014; Hamada et al., 2013). Baseline MEP am-
plitudes were also compared be tween groups using a
two-tailed independent samples t test to ensure that there
was no baseline difference between groups.
The stability of MEP amplitudes across the three time
points post-cTBS was determined using a one way re-
peated-measures ANOVA. To see if the MEP values were
reliable as well as stable over time post-cTBS, a correla-
tion analysis between the average MEP amplitudes for
each participant at each time point was conducted for
all pairwise combinations of time point (e.g., T1 vs. T2,
T2 vs. T3, T1 vs. T3). To determine whether MEP ampli-
tudes were consistently decreased or increased within
participants dependent on their overall categorization
into either the inhibitory or facilitatory groups, nonpara-
metric sign tests were conducted between the difference
in MEP amplitude from baseline at each time point and
the grand average difference in MEP amplitude from
baseline (used to categorize participants).
Behavioral Data Analysis
Confidence ratings were ordered based on ET from fast-
est to slowest and grouped into 10 bins per participant.
ET bins were divided to have as close to equal numbers
as possible. The first block, which had a total of 190
videos, had 19 in each bin, and the second block with
Palmer et al. 2023

192 videos had 19 in Bins 19 and 21 in the last bin. The
range of ETs in each bin were as follows: 8631023 msec
(Bin 1); 10231064 msec (Bin 2); 10681103 msec (Bin 3);
11031128 msec (Bin 4); 11291154 msec (Bin 5); 1154
1178 msec (Bin 6); 11781223 msec (Bin 7); 12241 259 msec
(Bin 8); 12691325 msec (Bin 9); 13291655 msec (Bin 10).
The mean confidence rating of each bin was plotted
against ET. The gradient of this line was used as a mea-
sure of sensitivity to movement speed. The mean confi-
dence rating across conditions for each participant was
deducted from the mean confidence rating at each bin
for each condition for each participant to normalize the
scores and remove any between-subject variance in use
of the confidence scale.
The outcome measure change in gradient (difference
in gradient [sensitivity] before and after cTBS) was ana-
lyzed between participants (inhibition and facilitation
grou ps based on change in mean MEP amplitude po st-
cTBS) using a two-tailed independent samples t tes t.
Post hoc tests were then carried out to provide more
details about the specificities of this effect. One-sample
t tests were conducted to identify whether the change
in gradient for each group was significantly different
from zero. Nonparametric permutation tests were also
conducted to corroborate the findings from the para-
metric tests using a statistical test that makes no assump-
tion as to the u nderlying distribution of th e observed
data. Here, for the change in gradient data, the condition
labels (inhibition group o r facilitation group) were ran-
domly permuted and the group mean difference calcu-
lated 1,000,000 times. Only unique group means were
selected in ensuring that the permuted distribution was
not biased. The distribution of mean differences was cal-
culated, and the position of the true mean difference was
determined to identify if the difference between the
groups was significant. The same analysis was conducted
separately for the inhibition and facilitation groups using
the pre- and post-cTBS data points to determine in each
group if the change in gradient observed was significantly
increased or decreased from zero. Baseline sensitivity to
observed movement speed before cTBS was also com-
pared between groups using a two-tailed independent
samples t test to ensure that there was no baseline differ-
ence between groups.
A linear regression analysis was used to determine the
predictive relationship between (1) observed movement
speed and inferred confidence ratings, and (2) change
in mean MEP amplitude and change in gradient. Although
there are alternative predictions one could make regard-
ing the shape of these relationships, based on previous
literature (Patel et al., 2012), for the purpose of this study
these relationships are assumed to be linear.
The response to indicate confidence required a motor
action with higher confidence ratings requiring a greater
number of key presses along the 0100 scale bar. To en-
sure that any changes in sensitivity to movement speeds
werenotcausedsimplybyanimpairmentatthemotorlevel
reducing the overall number of key presses produced, mean
confidence ratings in the fastest three time bins (highest
confidence ratings) were compared before and after cTBS
using paired sample t tests for the inhibition group. For
all outcome measures, assumption of a normal distribution
(using the Shapiro-Wilk test of normality) was verified.
RESULTS
Effect of cTBS on CSE
MEPs recorded from the right FDI of each participant be-
fore and after cTBS provided a physiological measure of
the efficacy of cTBS in disrupting the motor cortex. The
change in cortical excitability following cTBS was highly
variable between participants and over time in an individ-
ual participant. Representative MEP waveforms averaged
ove r 20 MEPs (baseline) or the grand average (3 × 20
MEPs) post-cTBS are shown from two individuals, which
had differential responses to cTBS (Figure 2A, 2B). Of 24
participants, 1 5 showed post-cTBS inhibition (mean ±
SD: 37.2 ± 21.4% decrease) and 9 showed post-cTBS fa-
cilitation (42.8 ± 29.6% increase; Figure 2C) defined by a
positive or negative change in the grand average post-
cTBS MEP amplitude from baseline (see Methods for
more details on categorization). There were no signifi-
cant differences between the two groups in b aseline
MEP amplitude, t(22) = 0.817, p = .423 (mean differ-
ence in MEP amplitude: 0.15 ± 0.09 mV) before cTBS.
To ensure MEP amplitudes were stable across time
points poststimulation, a one-way repeated-measures
ANOVA was conducted; this revealed no significant main
effect of Time, and none of the pairwise comparisons were
significant ( p > .1). Correlation analyses, conducted to
determine the reliability of the MEP amplitudes over time
post-cTBS, revealed significant positive rel ationships be-
tween average MEP amplitudes at all time points (T1 vs.
T2: r =.71,p < .001; T2 vs. T3: r =.54,p =.018;T1vs.
T3: r =.65,p < .001). Moreover, sign tests conducted to
determine whether MEP amplitudes were consistently
decreased or increased, dependent on their overall cate-
gorization into either the inhibition or facilitation groups,
were all significant (T1: p = .0075; T2: p = .0034; T3: p =
.0063), which demonstrates that the sign of the differ-
ence between the average MEP a mplitude at each time
point and the baseline MEP amplitude was consistently
the same as the sign associated with the group into which
participants were categorized.
Effect of cTBS on Sensitivity to Action Kinematics
ETs from all the videos shown were divided into 10 bins,
and the mean confidence rating across all participants for
each bin was plotted before and after cTBS (see Figure 3).
In all cases, movement speed significantly predicted inferred
confidence ratings, r
2
= .98, F(1, 237) = 472.37, p < .001;
as observed movement speed increased, participants
2024 Journal of Cognitive Neuroscience Volume 28, Number 12

Figure 2. Changes in CSE
following cTBS. MEPs recorded
from the right FDI muscle
before and after stimulation.
Mean baseline (blue) MEP
waveform averaged over
20 MEPs for each participant.
Post-cTBS (red = inhibition;
green = facilitation) MEP
waveforms averaged across
three time points following
cTBS (n = 60 MEPs).
(A) Representative mean
(SEM = shaded area) MEP
waveform before stimulation
(blue) and after stimulation
(red) from a participant in
the inhibition group.
(B) Representative mean
(SEM = shaded area) MEP
waveform before stimulation
(blue) and after stimulation
(green) from a participant
in the facilitation group.
(C) Mean (SEM ) percentage
change in MEP amplitude for
the inhibition group (red) and
the facilitation group (green).
S = stimulus artifact.
Figure 3. cTBS reduces
sensitivity to observed
kinematic information in
inhibition group. Mean
confidence ratings for observed
ETs were divided into 10 bins
before cTBS (solid line) and
after cTBS (dashed line).
Movement speed significantly
predicted inferred confidence
ratings for all graphs, r
2
= .98,
F(1, 237) = 472.37, p < .001.
(A) Mean (SEM ) confidence
ratings for observed ETs for
the inhibition group only
before and after cTBS.
Significant change in gradient
(measure of sensitivity) before
and after cTBS, t(14) = 2.25,
p = .041 (mean ± SD change
in gradient = 0.0095 ±
0.016). (B) Mean (SEM )
confidence ratings for observed
ETs for the facilitation group
only before and after cTBS. No
significant change in gradient
(measure of sensitivity) before
and after cTBS, t(8) = 0.92,
p = .39 (mean ± SD change in
gradient = 0.0041 ± 0.013).
(C) Change i n gradient (sensitivity) following cTBS for the inhibition group (red) and facilitation group (green). There was a significant
between-subject difference in change in sensitivity, t(22) = 2.1, p = .047. The facilitation group did not show a significant change in sensitivity
from 0, t(8) = 0.92, p = .39 (mean ± SD change in gradient = 0.0041 ± 0.013).
Palmer et al. 2025

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38 citations


Cites background from "A causal role for primary motor cor..."

  • ...A growing literature shows that the effect of brain stimulation is highly variable across individuals (Ridding and Ziemann, 2010; Jones et al., 2016; Palmer et al., 2016; Avenanti et al., 2018; Valchev et al., 2016, 2017; Paracampo et al., 2018)....

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Journal ArticleDOI
TL;DR: It is found that tDCS over mPFC - but not occipital or sham tDCS - decreased the propensity to mind-wander, and gender-related differences in tDCS-induced changes suggest that mP FC controls mind-Wandering differently in men and women, which may depend on differences in the structural and functional organization of distributed brain networks governing mind- wandering.
Abstract: Mind-wandering, the mind’s capacity to stray from external events and generate task-unrelated thought, has been associated with activity in the brain default network. To date, little is understood about the contribution of individual nodes of this network to mind-wandering. Here, we investigated the role of medial prefrontal cortex (mPFC) in mind-wandering, by perturbing this region with transcranial direct current stimulation (tDCS). Young healthy participants performed a choice reaction time task both before and after receiving cathodal tDCS over mPFC, and had their thoughts periodically sampled. We found that tDCS over mPFC - but not occipital or sham tDCS - decreased the propensity to mind-wander. The tDCS-induced reduction in mind-wandering occurred in men, but not in women, and was accompanied by a change in the content of task-unrelated though, which became more related to other people (as opposed to the self) following tDCS. These findings indicate that mPFC is crucial for mind-wandering, possibly by helping construction of self-relevant scenarios capable to divert attention inward, away from perceptual reality. Gender-related differences in tDCS-induced changes suggest that mPFC controls mind-wandering differently in men and women, which may depend on differences in the structural and functional organization of distributed brain networks governing mind-wandering, including mPFC.

38 citations

Journal ArticleDOI
TL;DR: Neuromodulation and lesion studies that address how activations in the mirror neuron system contribute to the authors' perception of observed actions are reviewed, suggesting embodied representations are somatosensory-motor.
Abstract: We review neuromodulation and lesion studies that address how activations in the mirror neuron system contribute to our perception of observed actions. Past reviews showed disruptions of this parieto-premotor network impair imitation and goal and kinematic processing. Recent studies bring five new themes. First, focal perturbations of a node of that circuit lead to changes across all nodes. Second, primary somatosensory cortex is an integral part of this network suggesting embodied representations are somatosensory-motor. Third, disturbing this network impairs the ability to predict the actions of others in the close (∼300ms) future. Fourth, disruptions impair our ability to coordinate our actions with others. Fifth, disrupting this network, the insula or cingulate also impairs emotion recognition.

38 citations

References
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Journal ArticleDOI
01 Apr 1996-Brain
TL;DR: It is proposed that mirror neurons form a system for matching observation and execution of motor actions, similar to that of mirror neurons exists in humans and could be involved in recognition of actions as well as phonetic gestures.
Abstract: We recorded electrical activity from 532 neurons in the rostral part of inferior area 6 (area F5) of two macaque monkeys. Previous data had shown that neurons of this area discharge during goal-directed hand and mouth movements. We describe here the properties of a newly discovered set of F5 neurons ("mirror neurons', n = 92) all of which became active both when the monkey performed a given action and when it observed a similar action performed by the experimenter. Mirror neurons, in order to be visually triggered, required an interaction between the agent of the action and the object of it. The sight of the agent alone or of the object alone (three-dimensional objects, food) were ineffective. Hand and the mouth were by far the most effective agents. The actions most represented among those activating mirror neurons were grasping, manipulating and placing. In most mirror neurons (92%) there was a clear relation between the visual action they responded to and the motor response they coded. In approximately 30% of mirror neurons the congruence was very strict and the effective observed and executed actions corresponded both in terms of general action (e.g. grasping) and in terms of the way in which that action was executed (e.g. precision grip). We conclude by proposing that mirror neurons form a system for matching observation and execution of motor actions. We discuss the possible role of this system in action recognition and, given the proposed homology between F5 and human Brocca's region, we posit that a matching system, similar to that of mirror neurons exists in humans and could be involved in recognition of actions as well as phonetic gestures.

4,358 citations


"A causal role for primary motor cor..." refers background in this paper

  • ...The majority of studies in this field have tested the hypothesis that motor system activity in some way facilitates the perception of the observed action goal (Ferrari, Rozzi, & Fogassi, 2005; Gallese et al., 1996)....

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  • ...Initial studies of mirror neurons (Gallese et al., 1996; di Pellegrino et al., 1992) did not find any evidence of these neurons in M1, and it was therefore assumed that M1 had no role at all in action perception....

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  • ...Initial studies of mirror neurons (Gallese et al., 1996; di Pellegrino et al., 1992) did not find any evidence of these neurons...

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Journal ArticleDOI
20 Jan 2005-Neuron
TL;DR: A very rapid method of conditioning the human motor cortex using rTMS that produces a controllable, consistent, long-lasting, and powerful effect on motor cortex physiology and behavior after an application period of only 20-190 s is described.

3,211 citations


"A causal role for primary motor cor..." refers background in this paper

  • ...The AMT was used to determine the intensity of stimulator output for cTBS; the Magstim Rapid2 (Magstim) was used to find the AMT....

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  • ...AMT = 50.28 ± 7.44% of MSO (Magstim Rapid2; AMT > RMT due to different stimulators used)....

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  • ...Resting and active motor thresholds (RMT, AMT) were recorded for each participant....

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  • ...AMT was determined while participants produced a steady isometric contraction against an inert object to produce a constant EMG output at 10% of their maximum voluntary contraction....

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  • ...The stimulator output intensity for cTBS was 80% of AMT (Huang et al., 2005)....

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Journal ArticleDOI
TL;DR: It is reported here that many neurons of the rostral part of inferior premotor cortex of the monkey discharge during goal-directed hand movements such as grasping, holding, and tearing, which indicates that premotor neurons can retrieve movements not only on the basis of stimulus characteristics, but also on the based of the meaning of the observed actions.
Abstract: Neurons of the rostral part of inferior premotor cortex of the monkey discharge during goal-directed hand movements such as grasping, holding, and tearing. We report here that many of these neurons become active also when the monkey observes specific, meaningful hand movements performed by the experimenters. The effective experimenters' movements include among others placing or retrieving a piece of food from a table, grasping food from another experimenter's hand, and manipulating objects. There is always a clear link between the effective observed movement and that executed by the monkey and, often, only movements of the experimenter identical to those controlled by a given neuron are able to activate it. These findings indicate that premotor neurons can retrieve movements not only on the basis of stimulus characteristics, as previously described, but also on the basis of the meaning of the observed actions.

2,977 citations


"A causal role for primary motor cor..." refers background in this paper

  • ...Initial studies of mirror neurons (Gallese et al., 1996; di Pellegrino et al., 1992) did not find any evidence of these neurons in M1, and it was therefore assumed that M1 had no role at all in action perception....

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Journal ArticleDOI
26 Sep 1986-Science
TL;DR: The direction of movement was found to be uniquely predicted by the action of a population of motor cortical neurons that can be monitored during various tasks, and similar measures in other neuronal populations could be of heuristic value where there is a neural representation of variables with vectorial attributes.
Abstract: Although individual neurons in the arm area of the primate motor cortex are only broadly tuned to a particular direction in three-dimensional space, the animal can very precisely control the movement of its arm. The direction of movement was found to be uniquely predicted by the action of a population of motor cortical neurons. When individual cells were represented as vectors that make weighted contributions along the axis of their preferred direction (according to changes in their activity during the movement under consideration) the resulting vector sum of all cell vectors (population vector) was in a direction congruent with the direction of movement. This population vector can be monitored during various tasks, and similar measures in other neuronal populations could be of heuristic value where there is a neural representation of variables with vectorial attributes.

2,921 citations

Journal ArticleDOI
TL;DR: It is concluded that in humans there is a system matching action observation and execution that resembles the one recently described in the monkey.
Abstract: 1. We stimulated the motor cortex of normal subjects (transcranial magnetic stimulation) while they 1) observed an experimenter grasping 3D-objects, 2) looked at the same 3D-objects, 3) observed an experimenter tracing geometrical figures in the air with his arm, and 4) detected the dimming of a light. Motor evoked potentials (MEPs) were recorded from hand muscles. 2. We found that MEPs significantly increased during the conditions in which subjects observed movements. The MEP pattern reflected the pattern of muscle activity recorded when the subjects executed the observed actions. 3. We conclude that in humans there is a system matching action observation and execution. This system resembles the one recently described in the monkey.

2,195 citations

Frequently Asked Questions (2)
Q1. What contributions have the authors mentioned in the paper "A causal role for primary motor cortex in perception of observed actions" ?

Here, the authors tested the hypothesis that the primary motor cortex ( M1 ) may have a causal role in inferring information that is present in the kinematics of observed actions. A neurophysiological marker was used to quantify the extent of M1 disruption following cTBS and stratify their sample a priori to provide an internal control. 

Future work is necessary to tease apart the mechanistic role of M1 within this predictive coding account. The precise nature of the interplay between PMv and M1 during action observation should form the basis of future studies ; for example, paired-pulse conditioning can be used to determine the magnitude of disruption in the PMv in response to cTBS over M1 to confirm these conclusions. Future studies could aim to determine the specificity for M1 in the processing of kinematic actions. During action execution it has been suggested that neurons within the PMv encode the direction of an action in space necessary to acquire a specific target ( goal ) ; this information is then transmitted to M1 and combined with muscle and joint information to determine how that action would be carried out ( kinematics ).