Anticipatory Planning Reveals Segmentation of Cortical Motor Output During Action Observation
Advance Access publication August
Anticipatory Planning Reveals Segmentation of Cortical Motor Output During Action Observation
Loes Janssen 0 1 2
Bert Steenbergen 1
Richard G. Carson 3 4
0 Department of Clinical Epidemiology, VieCuri Medical Centre , Venlo, 5912 BL , The Netherlands
1 Behavioural Science Institute, Radboud University Nijmegen , Nijmegen, 6500 HE , The Netherlands
2 Donders Institute for Brain , Cognition and Behaviour
3 School of Psychology, Queen's University Belfast , Belfast, BT7 1NN , Northern Ireland
4 Trinity College Dublin, Trinity College Institute of Neuroscience and School of Psychology , Dublin 2 , Ireland
It has been argued that the variation in brain activity that occurs when observing another person reflects a representation of actions that is indivisible, and which plays out in full once the intent of the actor can be discerned. We used transcranial magnetic stimulation to probe the excitability of corticospinal projections to 2 intrinsic hand muscles while motions to reach and grasp an object were observed. A symbolic cue either faithfully indicated the required final orientation of the object and thus the nature of the grasp that was required, or was in conflict with the movement subsequently displayed. When the cue was veridical, modulation of excitability was in accordance with the functional role of the muscles in the action observed. If however the cue had indicated that the alternative grasp would be required, modulation of output to first dorsal interosseus was consistent with the action specified, rather than the action observed-until the terminal phase of the motion sequence during which the object was seen lifted. Modulation of corticospinal output during observation is thus segmented-it progresses initially in accordance with the action anticipated, and if discrepancies are revealed by visual input, coincides thereafter with that of the action seen.
human; motor cortex; reaching-grasping movement; transcranial magnetic stimulation; visuomotor
It is well established that observation of action is associated
with changes in the excitability of corticospinal projections to
muscles that would be engaged in replication of the
movements being observed
(Fadiga et al. 1995, 2005)
variations are functionally and temporally specific—the amplitude
of responses to transcranial magnetic stimulation (TMS)
recorded from the first dorsal interosseus (FDI) muscle of a
passive observer is modulated in phase with the grip aperture
exhibited by an actor seen to approach and lift an object
(Gangitano et al. 2001). Furthermore, they may be anticipatory
in nature, thus providing for predictive coding of the behavior
(Kilner et al. 2004; Borroni et al. 2005; Aglioti et al.
2008; Urgesi et al. 2010; Alaerts et al. 2012; Sartori et al. 2012)
The phenomenon has been attributed
(Rizzolatti and Fadiga
to a mirror system akin to that inferred on the basis of
single-cell recordings from frontal and parietal areas of
(Rizzolatti and Craighero 2004)
. There is
however a notable point of divergence. Animal studies suggest
that successive elements of the observed movement sequence
are encoded separately
(Fadiga et al. 2000; Fadiga and
Craighero 2003; Craighero et al. 2007)
. For example, in describing the
behavior of neurons in the ventral premotor cortex (area F5)
that were active during the observation of specific actions,
Gallese et al. (1996)
noted that these could be classified on the
basis of their level of discharge during the various phases of
the compound movement that was viewed. It has been further
demonstrated that subsets of neurons in this brain region
respond when the final phase of an evolving action is implied,
whereas others are responsive only when it is portrayed
explicitly (Umiltà et al. 2001).
In contrast, on the basis of evidence derived from
noninvasive cortical stimulation, it has been argued that human
observers represent action sequences as indivisible ensembles
(Gangitano et al. 2004; Fadiga et al. 2005; Hauk et al. 2008;
Cattaneo and Rizzolatti 2009)
. Gangitano et al. (2004) reported
that the variations in corticospinal excitability exhibited
typically during observation of a reach to grasp movement, are not
obtained when the action does not proceed as expected
(delayed maximum aperture of the fingers or premature
closure of the hand). The authors concluded that “resonant
motor plan(s),” formed initially upon viewing the start of a
movement sequence, are neither modulated nor substituted
when the observed action does not proceed accordingly. It has
been inferred that instead they are suppressed if the visual
characteristics of the observed movement fail to match those
that are anticipated
(Gangitano et al. 2004)
In exploring observation-to-execution mappings expressed
via the human motor system, it has been noted that when the
intrinsic properties (e.g., the ostensible level to which a vessel
is filled) of an object, and the kinematic characteristics of its
manipulation (i.e., when seen lifted) are in conflict,
corticospinal output is modulated in accordance with kinematic rather
than object-related cues
(Alaerts et al. 2010)
. At first glance,
this might suggest that the engagement of the cortical motor
network strictly mirrors only the motor output characteristics
of the observed actions
(Cavallo et al. 2012)
. There is however
evidence that these processes are also subject to cognitive
penetration. When semantic information (e.g., a “light” or “heavy”
label) conflicts with the physical characteristics of the object of
an observed action, modulation of corticospinal output is
reduced, but not reversed
(Senot et al. 2011)
. It has thus been
proposed that—as when the observed action fails to match that
which is anticipated
(Gangitano et al. 2004)
, when semantic
and movement-related cues are in conflict, corticospinal
output is gated rather than regulated in accordance with
(Senot et al. 2011)
We reasoned that prior symbolic cues—if action oriented,
could in principle be used to establish whether human
observers represent action sequences as indivisible ensembles
or if successive elements of a movement sequence are encoded
separately. In contrast to approaches in which variants of
a single action (e.g., a precision grasp) have been used
(e.g,. Gangitano et al. 2004; Senot et al. 2011)
, the potential
segmentation of corticospinal excitability was considered in
the context of alternative actions that in their implementation
required different patterns of muscle engagement. This was
achieved by utilizing the phenomenon of anticipatory
movement planning—when preparing to grasp an object, account is
taken not only of its current configuration, but also of the
demands associated with the goal of the prospective action
(Johnson-Frey et al. 2004)
. Critically, this planning occurs not
only when movements are executed, but also when observed
(e.g., Flanagan and Johansson 2003)
Participants watched videos of actors performing object
manipulations using either a precision or whole-hand grasp. Prior
to movement initiation, a symbolic cue indicated the final goal
of the action. On this basis, the required grasp could be
inferred. In some instances (incongruent condition), the cue was
in conflict with the action that was subsequently displayed.
During each trial, motor-evoked potentials (MEPs) were
evoked in 2 hand muscles differentially engaged in precision
and whole-hand grasps, at 1 of 6 intervals defined relative to
the unfolding action sequence.
Critically, mapping a specific cue to a distinct action
provided the means of establishing the extent to which (in the
incongruent cue condition) the modulation of corticospinal
excitability unfolded in accordance with one alternative (i.e.,
the cued action) or the other alternative (i.e., the observed
action). The specific power of this design lies in the facility to
not only detect a deviation from the modulation associated
with the action that was cued (as in single action designs), but
also to establish (through the use of inferential tests of
equivalence) whether there was reversion to the pattern of modulation
associated with the alternative action (i.e., that being
observed). Our findings revealed that the variation of
corticospinal output that occurs during passive observation progresses
initially in accordance with the action that is anticipated, and if
discrepancies are revealed by visual input, coincides thereafter
with that of the action seen. The elements of observed
movement sequences are thus encoded separately.
Materials and Methods
Thirteen healthy right-handed adults (6 males) aged 18–38 years gave
written informed consent to the procedures, which were approved by
the local ethical committee and conducted in accordance with the
Declaration of Helsinki.
Twelve videos displayed an actor reaching for and grasping an object,
which was then inserted into 1 of 2 holes in a wooden block (Fig. 1).
The object was a black bar (diameter 14 mm, length 70 mm) attached
at one end to the center of a white disk (diameter 108 mm, thickness
12 mm). It could be grasped easily with either a precision grasp—on
the black bar, or whole-hand grasp—on the white disc. The block had
a small hole in which the black bar fitted precisely, and a large hole in
which the white disc fitted precisely. Comfortable insertion of the
object into the small hole required a whole-hand grasp of the white
disc. Insertion of the object into the large hole required a precision
grasp of the black bar. An arrow between the 2 holes could point
either to the small hole (whole-hand grasp required), or to the large
hole (indicating a precision grasp), or between the holes (no indication
of the required action).
Videos commenced with the object in a holder, the block positioned
to the left, and the actor’s prone (right) hand to the right (Fig. 1).
Theblock was oriented with the small hole on the left and the large
hole on the right, or vice versa. After 1000 ms, a yellow ring (diameter
100 mm) around the arrow appeared for 2000 ms to highlight the goal
cue. The hand started moving 3000 ms following the disappearance of the
ring and subsequently reached and grasped the object either by holding
the black bar (precision grasp) or the white disc (whole-hand grasp).
In the majority of trials (67%), the grasp was in accordance with the
goal cue (congruent). In some (22%) trials, however, the grasp
conflicted with the cue (incongruent). We also included “no-cue” trials
(11%) in which the arrow provided no indication of the required action
—the actor used either a precision or a whole-hand grasp to insert the
object in the corresponding hole.
The 12 different videos comprised combinations of 3 cues
(congruent, incongruent, no-cue), 2 grasps ( precision, whole-hand), and 2
block orientations (small hole left, small hole right). All were of 10 480
ms duration, followed by the presentation of a black screen for 2000 ms.
Electromyography and TMS
The electromyographic (EMG) activity of the FDI and abductor digiti
minimi (ADM) of the right hand was recorded using bipolar surface
electrodes. EMG signals were amplified, filtered (30 Hz–1 kHz), and
digitized (16 bit) at a sampling rate of 5000 Hz.
The FDI and ADM muscles perform functional roles in relation to
prehensile movements that are differentiated by the nature of the grasp
that must be formed. As the FDI acts as a principal agonist (abducts
and flexes the index finger) in precision grasps requiring index-thumb
opposition, it is engaged to a greater degree than in whole-hand
grasps—unless a clockwise rotation must be imparted upon the object
. The ADM assumes a significant functional role in
grasping large objects (such as the disc used in the present study) with
outstretched fingers, and is engaged accordingly. While it is not typically
activated to a significant degree in a prototypical pinch opposition
between the thumb and index finger, there was an additional
component to the precision grasp required in the present study. When the
object was lifted with a grasp of the black bar, it was necessary to also
extend (and fan) digits 4 and 5—including the little finger, in order to
avoid contact with the support stand (Fig. 2). As there is a tendon
attachment from ADM to the extensor expansion, the muscle contributes
to proximal and distal interphalangeal extension, and is duly engaged
(Marzke et al. 1998)
TMS was delivered to the left primary motor cortex (M1) by a
Magstim 200 stimulator (Magstim, Carmarthenshire), using a (30-mm
internal loop diameter; 85-mm external loop diameter) figure of eight
coil. The optimal position to obtain a MEP in the right ADM was
located and reproduced by the following means. A spot was first
marked on the scalp 6 cm lateral and 2 cm anterior to the vertex
(i.e., left M1 hand area), and the coil oriented to induce posterior to
anterior current flow in relation to the presumed orientation of the
motor strip. The coil was then moved systematically around this initial
location in both anterior–posterior and medial–lateral directions, until
the largest response was obtained. A line defining the intersection of
the 2 loops of the stimulating coil was marked directly on the scalp. An
additional marking aligned with the long axis of the coil handle—
which bisected the first line, was also made. During the experiment,
these markings were used to maintain constant the position and
orientation of the coil. The lowest stimulation intensity at which MEPs with
peak-to-peak amplitude of at least 50 µV could be recorded in 3 of 5
trials was taken as resting motor threshold (RMT). Stimulation at this
intensity also evoked a MEP in right FDI. The level of stimulation used
subsequently was 120% RMT. At the beginning and at the end of the
session, 3 sets of 10 control MEPs were obtained.
The rationale in using a stimulus intensity of 120% RMT was to
generate MEPs (i.e., in the control condition) with amplitudes in the middle of
the range that can be obtained for the muscles in question. On the basis
of our own experience
(e.g., Carroll et al. 2001)
and that of others
Devanne et al. 1997)
, we were confident that by using this (i.e., fixed)
stimulation intensity in the context of action observation, there was
scope for the amplitude of the MEPs to increase or decrease. It was thus
unlikely that either floor or ceiling effects would be present.
The participants were first familiarized with the object manipulation
task. They were instructed to grasp the object with their right hand and
insert it into the hole in the block—as cued by the arrow (using a
precision or whole-hand grasp as appropriate). The participant was then
asked to close their eyes. The experimenter changed the orientation of
the block. Following a verbal go-signal, the participant opened their
eyes and performed the task again. This was repeated until the
participant completed 20 successive trials using the correct grasp. In
requiring that the participants first perform the task themselves, we were
guided by recent findings
(e.g., Olsson and Nyberg 2011)
that it is
necessary to have experienced a motor act in order that corresponding
brain regions are recruited when the action is seen being performed. It
has also been reported that cueing in the context of action observation
is effective only when there has been preceding experience linking a
given cue to a specific action performed
(Petroni et al. 2010)
The participants were instructed to attentively observe the videos
that were displayed on a computer screen positioned 1 m ahead. In a
randomly defined subset of trials (18 of 288), they were asked to
imitate the movement they had just observed. The purpose of the
imitation trials was to ensure that the participants remained engaged. As
they were unable to anticipate whether on any given trial they would
be required to imitate the movement they had just observed, we
194 Anticipatory Planning
reasoned that this arrangement would ensure that the level of attention
allocated on every observation trial would be comparable. As there
were no errors in imitation, we are confident that the inclusion of this
requirement achieved the desired outcome. In most respects, the
procedure was similar to that employed during initial practice. There was
one key exception. The interleaved test movements were executed
using the left hand rather than the right hand. It was anticipated that
any action associated changes in the excitability of corticospinal
projections to the muscles of the hand performing the interleaved movement,
would have minimal impact upon the excitability of the projections to
the right hand that were assessed during the observation trials. Short
breaks were scheduled after each of the 18 imitation trials. Thus on
average, breaks were taken after sets of 16 observation trials.
During each observation trial, TMS was delivered in 1 of 6 phases
(delays): termination of the goal cue (3000 ms); 100 ms before
movement onset (4900 ms); just after movement onset but grasp as yet
unrevealed (5280 ms); maximal aperture of the precision grasp (5680 ms);
maximal aperture of the whole-hand grasp (6080 ms); during lifting of
the object prior to transport (7280 ms). In order to ensure precision of
timing for stimulus delivery, a discrete pulse was encoded on an audio
channel of the video file. The rising edge of this pulse was used to
trigger the TMS. To limit the total duration, and maintain a high
congruent/incongruent trial ratio—thus ensuring the integrity of any
associated internal models
(Schiffer et al. 2012)
, we administered TMS
in all 6 phases during congruent trials, in 4 phases during incongruent
trials, and in 2 phases during no-cue trials. As the videos for the
congruent and incongruent trials were identical during the movement
preparation phases (Fig. 1), we elected not to obtain MEPs at 3000 and
4900 ms in the latter condition. As the no-cue trials acted as a control,
principally with respect to the preparation phase, we administered
TMS only at 3000 (termination of the goal cue) and 4900 ms (100 ms
before movement onset). The 24 congruent combinations (4 videos × 6
delays) were repeated 8 times (total 192), the 16 incongruent
combinations (4 videos × 4 delays) 4 times (total 64), and the 8 no-cue
combinations (4 videos × 2 delays) 4 times (total 32). The order was
Data Reduction and Analyses
The amplitude of MEPs recorded in right FDI and ADM, and the
background EMG (root mean squared) 100 ms prior to each stimulus, was
calculated. If the background EMG in either muscle exceeded 10 µV,
the corresponding MEPs for both muscles were excluded. Overall, 97%
of trials were retained. There were no systematic differences between
conditions in this regard. The amplitudes of MEPs recorded during
observation were normalized separately for each participant with
respect to the responses obtained at the beginning and end of each
session (the data values obtained prior to normalization are reported in
Tables 1 and 2). Thus normalized values >1 (i.e., Fig. 4) represent an
elevation of MEP amplitude relative to that obtained in the control
Inferential tests of difference consisted of a series of theoretically
meaningful preplanned comparisons
(e.g., Keppel 1991)
. These were
F-tests, whereby an omnibus ANOVA (repeated measures) model was
used to derive the sums of squares and means squares relevant to each
comparison. Corresponding effect sizes (f ) were also obtained
. In addition, an inferential test of equivalence
, specifically the paired t-test for equivalence (Wellek
2010), was calculated for each comparison. As the equivalence tests are
disjoint with the tests of difference, both can be applied using the
same alpha criterion (i.e., 0.05). A summary of outcomes of these
comparisons is given in Tables 3–6.
Muscle Activity During Execution of the Movement Task
In a supplementary experiment, we established the patterns of activity
in FDI and ADM during execution of the 2 variants of the task. For this
purpose, we engaged a further 5 participants and asked them to each
perform 10 instances of the full grasp action and 10 instances of the
precision grasp action. The EMG recordings were normalized in time
with respect to the onset and offset of the movement derived from a
video record. The amplitude of each (enveloped (50 Hz) and rectified)
EMG record was normalized with respect to the maximum value
obtained on that individual trial.
As inspection of Figure 2 reveals, in the precision grasp variant of
the task, for ADM there is an initial interval of low amplitude activity as
the posture of the hand is modified, followed by a period of muscle
quiescence coinciding with the time of maximum aperture in the
whole-hand grasp condition. Thereafter, activity in ADM increased,
and was maintained at a relatively stable level through the lift phase.
This is in accordance with the requirement that the little finger be
extended to avoid contact with the support stand, as the object is lifted.
Activity in the FDI muscle was less conspicuously biphasic. In all
participants, the maximum level of engagement of FDI occurred just in
advance of the moment the object was lifted. In the whole-hand grasp
condition (Fig. 3), activity in the ADM muscle reached a maximum
following the time of maximum hand aperture, and declined thereafter
through the lift phase. In FDI, the maximum level of activity in this
condition was registered just in advance of the moment the object was
lifted. Notably, the overall level of activity and degree of modulation
recorded in FDI was markedly greater in the precision than in the
wholehand variant of the task. For the ADM muscle, at least in the period
before the object was lifted, the contrast was less conspicuous. There
was remarkable consistency across the participants in the degree to
which these patterns were expressed. These EMG data provide one
context in which to assess the variations in excitability of corticospinal
projections to FDI and ADM obtained during observation of the same
actions in the main experiment (as described below).
Each phase was defined by the time of stimulation relative to onset of the trial. Note that for the Incongruent Cue conditions, the row labels indicate the action that was displayed.
2.42 ± 0.91
2.17 ± 0.87
2.43 ± 0.91
2.20 ± 1.06
0.61 ± 0.35
0.67 ± 0.43
0.60 ± 0.40
0.68 ± 0.54
Time of stimulation (ms)
2.24 ± 1.01
2.42 ± 1.22
2.36 ± 1.05
2.37 ± 1.18
Each phase was defined by the time of stimulation relative to onset of the trial. Note that for the Incongruent Cue conditions, the row labels indicate the action that was displayed.
We first examined situations in which no advance information
was provided concerning the action that might follow. In these
trials, MEPs were evoked at the termination of the (no) cue
phase, and 100 ms prior to the onset of movement. It was
verified that for FDI and ADM respectively, the amplitudes of the
MEPs elicited in the 2 phases did not vary systematically from
one another (F < 1, P > 0.20). On this basis, means were
obtained for each muscle (Fig. 4). These provided references with
respect to which the values obtained in the congruent and
incongruent conditions could be assessed.
It is important to note that the responses obtained following
the provision of a noninformative (but presumably alerting)
cue before the onset of the action then observed—were of
greater (≈140%) magnitude than those obtained in the controls
undertaken prior to and following the observation trials. This
reflects an anticipatory increase in corticospinal excitability in
the general context of cued action observation
Fernandez Del Olmo 2011)
. In relation to the effects of prior
symbolic cues indicating the nature of the action that would follow
(described in the sections below), these therefore reflect
muscle-specific and action goal-related variations of
corticospinal excitability superimposed upon the elevation attributable
to the generic requirements of the task.
When the observer saw a whole-hand grasp cued and executed
(Fig. 4A, triangles: dashed green line), MEPs elicited in FDI
diminished in amplitude following the onset of the actor’s
movement and reached their lowest point prior to the maximum
196 Anticipatory Planning
Cue: precision; Grasp: whole hand vs. Cue: whole hand; Grasp: whole hand
Post onset 0.63
Cue: precision; Grasp: whole hand vs. Cue: precision; Grasp: precision
Post onset 0.65
aperture of the grasp. When a precision grasp was specified
(Fig. 4A, diamonds: dashed blue line), a similar pattern of
modulation across phases was obtained; however, the excitability of
projections to this muscle was elevated to a greater degree. The
difference between the conditions was most pronounced at
the maximum aperture of the precision grasp (F1, 108 = 5.91,
P < 0.05, f = 0.23)—highlighted by filled symbols in Figure 4A.
The pattern of variation observed for ADM was distinct from
that of FDI, and consistent with the functional role of the
muscle in the actions observed. When a whole-hand grasp was
cued and demonstrated (Fig. 4B, triangles: dashed green line),
MEPs elicited in ADM were most elevated during maximum
aperture. Whereas, when a precision grasp was cued and
then seen performed (Fig. 4A, diamonds: dashed blue line),
ADM MEPs diminished in amplitude during this phase
(Fig. 4B). Thus, the greatest difference between conditions
coincided with the maximum aperture of the whole-hand
grasp (F1, 108 = 11.09, P < 0.01, f = 0.32)—highlighted by filled
symbols in Figure 4B.
In light of the functionally specific, variations in corticospinal
excitability present when the advance information and
following action were congruent, we sought to determine the pattern
of modulation exhibited when they were incongruent. If
successive elements of an observed movement sequence were
encoded separately, it would be anticipated that equivalence
tests would indicate that corticospinal output was initially in
concordance with the action cued, and subsequently (i.e., from
one point in time onward) equivalent to that associated with
the action that is seen.
When a whole-hand grasp was cued and a precision grasp
demonstrated subsequently (Fig. 4A, circles: solid purple line),
the amplitude of MEPs elicited in FDI matched initially those
obtained for the whole-hand grasp (i.e., correctly cued)
(Fig. 4A, triangles: dashed green line). The MEP amplitudes
were equated immediately following the onset of movement,
through to the phase during which the maximum aperture of a
whole-hand grasp would have been anticipated (P < 0.05).
This is highlighted by the green dashed ovals on Figure 4A
indicating values equivalent to those of the cue: whole-hand;
grasp: whole-hand condition (the outcomes of the
corresponding inferential analyses are given in the upper portion of
Table 3, first 3 rows). The sustained impact of the erroneous
advance information was such that: at the time the maximum
aperture of the precision grip was observed, the MEP
amplitudes remained markedly lower then those obtained when a
precision grasp was both cued and observed (F1, 108 = 4.34,
P < 0.05, f = 0.20), thus matching in this additional respect the
condition in which the observer saw a whole-hand grasp cued
and executed. During the final phase of the movement in
which the actor was seen to lift the object using a precision
grasp however, the MEPs were elevated in amplitude, such
that they were equivalent (P < 0.05) to those recorded in the
precision grasp (i.e., correctly cued) condition. This is
highlighted by the blue dashed oval on Figure 4A indicating a value
equivalent to that of the cue: precision; grasp: precision
condition (the outcome of the corresponding inferential test is
given in the lower portion of Table 3, final row).
A corresponding transition was evident if the advance
information indicated (erroneously) that a precision grasp would
follow (Fig. 4A, squares: solid red line). FDI MEPs were of
equivalent amplitude (P < 0.05) to those exhibited when a
precision grasp was both cued and executed (Fig. 4A,
diamonds: dashed blue line): during phases in which the
maximum aperture of a precision grasp would have been
anticipated, and the maximum aperture of the whole-hand
grasp was observed. This is highlighted by the blue dashed
ovals on Figure 4A indicating values equivalent to those of the
cue: precision; grasp: precision condition (the outcomes of the
corresponding inferential analyses are given in the lower
portion of Table 4, rows 2 and 3). In the former case, MEP
amplitudes were reliably greater than when a whole-hand grasp
was both cued and observed (F1, 108 = 4.79, P < 0.05, f = 0.21),
thus matching in this additional respect the condition in which
the observer saw a precision grasp cued and executed. During
the final lift phase of the depicted (whole-hand grasp) action,
the MEP amplitudes decreased to a level that could not be
discriminated (P < 0.05) from those obtained when the
(wholehand) cue and grasp were congruent (Fig. 4A). This is
highlighted by the green dashed oval on Figure 4A indicating a
value equivalent to that of the cue: whole-hand; grasp:
wholehand condition (the outcome of the corresponding inferential
test is given in the upper portion of Table 4, fourth row).
With respect to the FDI muscle therefore, the outcomes of
the inferential analyses corroborated the observation that
corticospinal output was initially in concordance with the action
anticipated, and subsequently equivalent to that associated
with the action that is seen. This was the case both in
circumstances in which a whole-hand grasp was cued and a precision
grasp then demonstrated, and when a precision grasp was
cued and a whole-hand grasp shown subsequently. These data
thus provide strong support for the hypothesis that successive
elements of an observed movement sequence are encoded
An incorrect cue having been presented, variations in the
excitability of projections to ADM were attenuated relative to
when the nature of the action had been pre-empted faithfully
(Fig. 4B). Thus, if a whole-hand grasp was cued and a
precision grasp demonstrated (Fig. 4B, circles: solid purple line),
the diminution of MEP amplitude through the max-precision
and max-whole-hand phases were less marked, than that
obtained when a precision grasp was cued and observed (Fig. 4B,
diamonds: dashed blue line). The attenuation was most
pronounced during the phase in which the maximum aperture of
a whole-hand grasp would have been anticipated (f = 0.21 vs.
0.32). The values obtained in the 2 conditions did however
tend towards convergence (i.e., for the incongruent condition
—correspondence with the action observed) during the final
(lift) phase of the sequence.
A consistent profile of attenuation—in this case relative to the
condition in which whole-hand grasp was cued and observed,
was expressed when a precision grasp was cued and a
wholehand grasp demonstrated. Thus, the potentiation of MEP
amplitude observed in the cue: precision; grasp: whole-hand
condition (Fig. 4B, squares: solid red line) was less marked through
the max-precision and max-whole-hand phases than that
obtained when a whole-hand grasp was cued and observed
(Fig. 4B, triangles: dashed green line). This effect was no longer
present during the final (lift) phase of the sequence.
In general therefore, the influence of the incongruent cue
appeared to be manifested (i.e., in modulation of MEP
amplitude) earlier for the ADM muscle than for FDI. Inspection of
the EMG profiles obtained for the real execution of the grasps
indicates that for both the precision and whole-hand variants,
198 Anticipatory Planning
activation of ADM occurred prior to that of FDI (Figs 2 and 3).
Thus, precocious changes in the excitability of corticospinal
projection to ADM are in accordance with the relative timing of
muscle engagement that is required to generate these
movements. Nonetheless, temporal segmentation of corticospinal
output in the incongruent conditions was expressed more
prominently for FDI than for ADM.
We used TMS to probe the excitability of corticospinal
projections to intrinsic hand muscles while motions to reach and
grasp an object were observed. Each action was preceded by a
symbolic cue that either faithfully indicated the required final
position of the object, and thus, the nature of the grasp that
was required, or was in conflict with the movement
subsequently displayed. When the cue was veridical, the
responses recorded from FDI and ADM were modulated in
accordance with their functional role in the action that was
(Gangitano et al. 2001)
. If however the symbolic cue
had indicated that the alternative grasp would be required, a
quite distinct pattern of modulation was obtained. When a
precision grasp was cued and a whole-hand grasp seen executed
subsequently, or a whole-hand grasp cued and a precision
grasp then displayed, the modulation of corticospinal output
to FDI was consistent with the action specified, rather than the
action observed—until the terminal phase of the motion
sequence during which the object was seen lifted. The
excitability of corticospinal projections to the ADM muscle was also
modified by advance information. When there was
incongruence between the action specified and the action observed, the
modulation of corticospinal output to ADM was attenuated
relative to that obtained when the cue faithfully represented
the required final position of the object.
When the ostensible intrinsic properties of an object (e.g.,
purported weight) and its motion are incongruent, the
variation in corticospinal output exhibited by an observer is
commensurate with the kinematics displayed rather than the forces
(Alaerts et al. 2010)
. If, however, there is a mismatch
between a semantic cue (an object labeled “heavy” or “light”)
and a weight-determined kinematic profile, modulation of
corticospinal excitability is diminished, and a general inhibition of
motor output pertains
(Senot et al. 2011)
. Similarly, if the
anticipated and observed kinematics are at odds, there occurs
abolition of the modulation associated with the anticipated
action, rather than substitution by a profile commensurate with
the observed motion. On this basis, it has been proposed that
resonant motor plans, primed as observation commences,
either proceed to completion or are suppressed as
inconsistencies are revealed subsequently by visual input
et al. 2004; Fadiga et al. 2005; Hauk et al. 2008; Cattaneo and
Unlike most previous investigations, we studied 2 alternative
grasp actions ( precision or whole-hand). The overall level of
activity and degree of modulation recorded in FDI during
execution was in accordance with its functional contribution,
and was thus markedly greater in the precision than in the
whole-hand variant of the task. While the level of ADM activity
present during execution of the 2 task variants was not
dissimilar, the temporal pattern of modulation was clearly
differentiated. In the whole-hand grasp, the ADM recruitment
contributed to the enclosure of the object, whereas when the
precision grasp was required, ADM activity served primarily to
extend the little finger to avoid contact with the support stand.
The observation of each grasp action also gave rise to a
distinct profile of corticospinal excitability. As in some instances
the prior symbolic cue misrepresented the grasp that would
then be depicted, this design offered the means to determine
whether, as the action unfolded, modulation of corticospinal
output proceeded in conformity with the grasp that was
anticipated, or was altered in accordance with the grasp that was
observed. Tests of equivalence provided the strong inferential
basis upon which to substantiate this determination. In
contrast to the conclusion presented elsewhere—that motor plans
once primed proceed through to completion, our findings
reveal that modulation of corticospinal output during passive
observation may progress first in accordance with the action
that is anticipated, and if discrepancies are revealed by visual
input, coincide thereafter with the action that is seen. This
phenomenon was expressed with particular clarity in relation
to the amplitude of motor potentials evoked in the FDI muscle.
Indeed, a single mean value diverged from the general pattern
(Fig. 4A). And yet for the ADM also, there was little evidence of
a pattern of modulation primed by the prior symbolic cue
proceeding independently of the observed action. Nor was there
an overall suppression of corticospinal output. Rather, there
was a transition to the profile of corticospinal excitability
designated by the motion seen, albeit at reduced gain.
Single-cell recordings from non-human primates have
revealed clusters of neurons in premotor regions that encode
distinct sequential elements of distal limb movements
et al. 1988; Rizzolatti and Fadiga 1998)
. Groups of cells in
ventral premotor cortex that discharge not only during the
execution of hand actions but also during their observation can
be differentiated on this basis (Gallese et al. 1996). Indeed,
subsets of neurons in this region remain engaged when the final
parts of an action sequence are not shown directly, but must be
inferred from the preceding elements (Umiltà et al. 2001). Prior
to the present study, there has been little direct evidence that a
similar segmentation of action sequence is expressed via the
human motor system during observation of others.
The manner in which an object is grasped is dependent on
the purpose of the action. The preference for a comfortable
joint-angle configuration at the end of the movement, even
when this necessitates an awkward posture when an object is
first approached, has been termed the end-state comfort effect
(Rosenbaum et al. 1992)
. Thus, when planning how to grasp
an object, account is taken of the prospective demands
associated with the goal of the action
(Johnson-Frey et al. 2004)
Such anticipatory planning implies that the purpose of a
movement is represented prior to encoding of the manner in which
it will be given effect.
The symbolic cue used in the present study indicated to the
observer the purpose of the action, and thus (indirectly) the
ultimate joint-angle configuration required for its realization.
The phases of movement giving rise to this outcome could be
inferred only on the basis of anticipatory planning.
Circumstances in which the cue is accurate cannot provide the means
upon which to determine whether these phases are
represented sequentially by the observer or as an ensemble. If
however the symbolic cue specifies one of a set of possible
outcomes, and an alternative is then shown, the modulation of
corticospinal output that occurs as the action unfolds provides
a basis for this determination. In this regard, the outcomes of
the present study reveal that humans exhibit temporal
segmentation in representing and anticipating the behavior of others.
Congruent spiking modulation of single units and
commensurate variations in local field potentials have been observed in
the primary motor cortex of macaques during action and
(Tkach et al. 2007)
. The changes in
corticospinal excitability registered via TMS when humans perform
similar tasks may reflect corresponding processes. That which
remains to be resolved is the causal status of fluctuations in
functional connectivity among elements of a wider brain
network that also includes the inferior frontal cortex (IFC;
ventral premotor cortex and inferior frontal gyrus), parietal
and temporal cortices, in mediating both concurrent and
anticipatory responses to the seen action of others.
In a recent study in which repetitive TMS (rTMS) was used
to transiently disrupt regions within IFC,
Avenanti et al. (2012)
reported abolition of the increases in corticospinal excitability
otherwise obtained when the actions of observed others
are implied by static pictures. In contrast, when rTMS was
delivered to the superior temporal sulcus (STS)—putatively a
relay linking “lower order” visual and frontoparietal regions
(e.g., Rizzolatti and Luppino 2001)
, the modulation of
corticospinal excitability was more pronounced. These data were
interpreted as support for the supposition that a reciprocal
control system is engaged in such tasks, whereby activity
registered initially in STS influences visuomotor (frontoparietal)
processing, which in turn alters information processing in
temporal regions. Of particular interest in the present context is
the more general hypothesis that information flow from
premotor to parietal and middle temporal cortices is determined
by the degree to which forward models (Kawato 1999) of
sensory consequences can be imputed from the observed
actions of others
(Schippers and Keysers 2011)
. As far as we
are aware there has not yet been an extension of this line of
reasoning to encompass the impact of such task-dependent
variations in functional connectivity on the state of circuits in
the primary motor cortex. There is however empirical evidence
to suggest that activity in presupplementary motor area
( pre-SMA) is elevated if prediction is required following
transient occlusion of an observed action
(Stadler et al. 2011)
. To the
extent that anticipatory and concurrent responses to the
viewed actions of others are mediated by distinct patterns of
functional connectivity in brain circuits that project to primary
motor cortex, a means of mediating the temporal segmentation
of corticospinal excitability observed in the present study is
provided, at least in principle.
There were differences between projections to the FDI and
ADM muscles in the degree to which this temporal
segmentation was expressed. In light of the contingent relation between
experience of a motor act and the brain activity that arises
during observation of that act
(e.g., Petroni et al. 2010; Olsson
and Nyberg 2011)
, a parsimonious account of this feature of
the data may be derived from our observation that the
differential modulation of EMG activity that occurs in the real
execution of the precision and whole-hand grasps is
considerably more pronounced for FDI than for ADM (Figs 2 and 3).
Nonetheless, there are other factors that may be implicated.
The features of a cortical circuit mediating visually guided
grasping, that comprises the anterior intraparietal area (AIP),
ventral premotor cortex (PMv), and M1 are now well
documented (Castiello 2005). There is a high degree of functional
specificity in the interactions between PMv and M1. Conditioning
TMS applied to PMv has larger impact upon projections from
M1 to FDI in the context of a precision grip, and a greater
influence on projections from M1 to ADM when a whole-hand
grasp is adopted
(Davare et al. 2010)
. The AIP plays a part in
mediating the integration of object specifications derived from
visual input as the shape of the hand is specified during
grasping. AIP activity is however much weaker during a whole-hand
grasp than a precision grasp
(Begliomini et al. 2007)
Corticomotoneuronal projections to FDI exhibit higher gain than
those to ADM
(Ziemann et al. 2004a, 2004b)
. Thus, whether
considered in relation to their descending projections, or the
task contexts in which they assume a primary functional role
( precision vs. whole-hand grip), the representations of FDI
and ADM are differentiated within the cortical circuits that
regulate visually guided grasping
(see also Ni et al. 2006)
corresponding distinction expressed during the observation of
action is therefore to be anticipated.
Is it conceivable that the effects observed in the incongruent
trials, particularly at the beginning of each trial, were
attributable to an influence of the symbolic cue that transcended the
anticipatory modulation of corticospinal excitability that was
expressed once the movement was seen to commence? MEPs
were elevated (relative to controls undertaken prior to and
following the observation trials) in the no-cue condition in which
the direction of the arrow provided no information concerning
the nature of the forthcoming action. A conspicuous feature of
the data presented in Tables 1 and 2 is the similarity of these
values to those obtained in the cued conditions at termination
of the goal cue (following a 2000 ms presentation) and 1900
ms thereafter (100 ms before movement onset). Indeed, in
none of these instances did a value obtained for the cued trials
( precision or whole-hand) for either FDI or ADM lie outside
the 95% confidence interval defined for the corresponding
no-cue trials. It appears therefore that the impact of a symbolic
cue on anticipatory movement planning becomes manifest
only upon initiation of the action that is witnessed.
Beyond the fundamental knowledge generated by the
present study, consideration might also be given to the
potential practical application of the findings in rehabilitation, for
example following stroke. It has been proposed previously
(e.g., Small et al. 2012)
that action observation and imitation
may prove beneficial in this context. The current outcomes, and
indeed those concerning the patterns of functional brain
connectivity that mediate concurrent and anticipatory responses to
the seen action of others, suggest that interventions based on
(e.g., Ertelt et al. 2007)
might be tailored—
through manipulation of specific task demands (e.g., the
requirements for anticipation), to the constellation of cerebral
damage sustained by individual stroke survivors.
Richard Carson thanks Atlantic Philanthropies for their generous
support of his research through their funding of the NEIL
(Neuroenhancement for Independent Lives) program at Trinity College Institute
of Neuroscience. Conflict of Interest: None declared.
200 Anticipatory Planning
Aglioti SM , Cesari P , Romani M , Urgesi C. 2008 . Action anticipation and motor resonance in elite basketball players . Nat Neurosci . 11 : 1109 - 1116 .
Alaerts K , de Beukelaar TT , Swinnen SP , Wenderoth N. 2012 . Observing how others lift light or heavy objects: time-dependent encoding of grip force in the primary motor cortex . Psychol Res . 76 : 503 - 513 .
Alaerts K , Swinnen SP , Wenderoth N. 2010 . Observing how others lift light or heavy objects: which visual cues mediate the encoding of muscular force in the primary motor cortex? Neuropsychologia . 48 : 2082 - 2090 .
Avenanti A , Annella L , Candidi M , Urgesi C , Aglioti SM . 2012 . Compensatory plasticity in the action observation network: virtual lesions of STS enhance anticipatory simulation of seen actions . Cereb Cortex . 23 : 570 - 580 .
Begliomini C , Wall MB , Smith AT , Castiello U. 2007 . Differential cortical activity for precision and whole-hand visually guided grasping in humans . Eur J Neurosci . 25 : 1245 - 1252 .
Borroni P , Montagna M , Cerri G , Baldissera F. 2005 . Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement . Brain Res . 1065 : 115 - 124 .
Carroll TJ , Riek S , Carson RG . 2001 . Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation . J Neurosci Meth . 112 : 193 - 202 .
Castiello U. 2005 . The neuroscience of grasping . Nat Rev Neurosci . 6 : 726 - 736 .
Cattaneo L , Rizzolatti G. 2009 . The mirror neuron system . Arch Neurol . 66 : 557 - 560 .
Cavallo A , Becchio C , Sartori L , Bucchioni G , Castiello U. 2012 . Grasping with tools: corticospinal excitability reflects observed hand movements . Cereb Cortex . 22 : 710 - 716 .
Cohen J. 1969 . Statistical power analysis for the behavioral sciences . Hillsdale , NJ: Lawrence Erlbaum.
Craighero L , Metta G , Sandini G , Fadiga L. 2007 . The mirror-neurons system: data and models . Prog Brain Res . 164 : 39 - 59 .
Davare M , Rothwell JC , Lemon RN . 2010 . Causal connectivity between the human anterior intraparietal area and premotor cortex during grasp . Curr Biol . 20 : 176 - 181 .
Devanne H , Lavoie BA , Capaday C. 1997 . Input-output properties and gain changes in the human corticospinal pathway . Exp Brain Res . 114 : 329 - 338 .
Ertelt D , Small S , Solodkin A , Dettmers C , McNamara A , Binkofski F , Buccino G. 2007 . Action observation has a positive impact on rehabilitation of motor deficits after stroke . Neuroimage . 36 : T164 - T173 .
Fadiga L , Craighero L. 2003 . New insights on sensorimotor integration: from hand action to speech perception . Brain Cogn . 53 : 514 - 524 .
Fadiga L , Craighero L , Olivier E. 2005 . Human motor cortex excitability during the perception of others' action . Curr Opin Neurobiol . 15 : 213 - 218 .
Fadiga L , Fogassi L , Gallese V , Rizzolatti G. 2000 . Visuomotor neurons: ambiguity of the discharge or “motor” perception? Int J Psychophysiol . 35 : 165 - 177 .
Fadiga L , Fogassi L , Pavesi G , Rizzolatti G. 1995 . Motor facilitation during action observation: a magnetic stimulation study . J Neurophysiol . 73 : 2608 - 2611 .
Flanagan JR , Johansson RS . 2003 . Action plans used in action observation . Nature . 424 : 769 - 771 .
Gallese V , Fadiga L , Fogassi L , Rizzolatti G. 1996 . Action recognition in the premotor cortex . Brain . 119 ( Pt 2 ): 593 - 609 .
Gangitano M , Mottaghy FM , Pascual-Leone A. 2004 . Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements . Eur J Neurosci . 20 : 2193 - 2202 .
Gangitano M , Mottaghy FM , Pascual-Leone A. 2001 . Phase-specific modulation of cortical motor output during movement observation . Neuroreport . 12 : 1489 - 1492 .
Hauk O , Shtyrov Y , Pulvermüller F. 2008 . The time course of action and action-word comprehension in the human brain as revealed by neurophysiology . J Physiol Paris. 102 : 50 - 58 .
Johnson-Frey SH , McCarty ME , Keen R. 2004 . Reaching beyond spatial perception: effects of intended future actions on visually guided prehension . Visual Cogn . 11 : 371 - 399 .
Kawato M. 1999 . Internal models for motor control and trajectory planning . Curr Opin Neurobiol . 9 : 718 - 727 .
Keppel G. 1991 . Design and analysis: a researcher's handbook . Englewood Cliffs J : Prentice-Hall .
Kilner JM , Vargas C , Duval S , Blakemore S-J , Sirigu A. 2004 . Motor activation prior to observation of a predicted movement . Nat Neurosci . 7 : 1299 - 1301 .
Lago A , Fernandez Del Olmo M. 2011 . Movement observation specifies motor programs activated by the action observed objective . Neurosci Lett . 493 : 102 - 106 .
Long C. 1981 . Electromyographic studies of hand function . In: Raoul T, editor. The Hand . Vol. 1 . Philadelphia: W.B. Saunders. p. 427 - 440 .
Marzke MW , Toth N , Schick K , Reece S , Steinberg B , Hunt K . et al. 1998 . EMG Study of hand muscle recruitment during hard hammer percussion manufacture of oldowan tools . Am J Phys Anthropol . 105 : 315 - 332 .
Ni Z , Takahashi M , Yamashita T , Liang N , Tanaka Y , Tsuji T . et al. 2006 . Functional demanded excitability changes of human hand motor area . Exp Brain Res . 170 : 141 - 148 .
Olsson C-J , Nyberg L. 2011 . Brain simulation of action may be grounded in physical experience . Neurocase . 17 : 501 - 505 .
Petroni A , Baguear F , Della-Maggiore V. 2010 . Motor resonance may originate from sensorimotor experience . J Neurophysiol . 104 : 1867 - 1871 .
Rizzolatti G , Camarda R , Fogassi L , Gentilucci M , Luppino G , Matelli M. 1988 . Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements . Exp Brain Res . 71 : 491 - 507 .
Rizzolatti G , Craighero L. 2004 . The mirror-neuron system . Annu Rev Neurosci . 27 : 169 - 192 .
Rizzolatti G , Fadiga L. 1998 . Grasping objects and grasping action meanings: the dual role of monkey rostroventral premotor cortex (area F5) . Novartis Found Symp . 218 : 81 - 95 ; discussion 95- 103 .
Rizzolatti G , Luppino G. 2001 . The cortical motor system . Neuron . 31 : 889 - 901 .
Rosenbaum DA , Vaughan J , Barnes HJ , Jorgensen MJ . 1992 . Time course of movement planning: selection of handgrips for object manipulation . J Exp Psychol Learn Mem Cogn . 18 : 1058 - 1073 .
Sartori L , Bucchioni G , Castiello U. 2012 . Motor cortex excitability is tightly coupled to observed movements . Neuropsychologia . 50 : 2341 - 2347 .
Schiffer A-M , Ahlheim C , Ulrichs K , Schubotz RI . 2012 . Neural changes when actions change: adaptation of strong and weak expectations . Hum Brain Mapp . 34 : 1713 - 1727 .
Schippers MB , Keysers C. 2011 . Mapping the flow of information within the putative mirror neuron system during gesture observation . Neuroimage . 57 : 37 - 44 .
Senot P , D'Ausilio A , Franca M , Caselli L , Craighero L , Fadiga L. 2011 . Effect of weight-related labels on corticospinal excitability during observation of grasping: a TMS study . Exp Brain Res . 211 : 161 - 167 .
Small SL , Buccino G , Solodkin A. 2012 . The mirror neuron system and treatment of stroke . Dev Psychobiol . 54 : 293 - 310 .
Stadler W , Schubotz RI , Cramon von DY , Springer A , Graf M , Prinz W. 2011 . Predicting and memorizing observed action: differential premotor cortex involvement . Hum Brain Mapp . 32 : 677 - 687 .
Tkach D , Reimer J , Hatsopoulos NG . 2007 . Congruent activity during action and action observation in motor cortex . J Neurosci . 27 : 13241 - 13250 .
Umiltà MA , Kohler E , Gallese V , Fogassi L , Fadiga L , Keysers C , Rizzolatti G. 2001 . I know what you are doing. A Neurophysiological Study . Neuron . 31 : 155 - 165 .
Urgesi C , Maieron M , Avenanti A , Tidoni E , Fabbro F , Aglioti SM . 2010 . Simulating the future of actions in the human corticospinal system . Cereb Cortex . 20 : 2511 - 2521 .
Wellek S. 2010 . Testing statistical hypotheses of equivalence and noninferiority . Boca Raton, Fl: Chapman & Hall.
Wellek S , Michaelis J. 1991 . Elements of significance testing with equivalence problems . Methods Inform Med . 30 : 194 - 198 .
Ziemann U , Ilic TV , Alle H , Meintzschel F. 2004a . Cortico-motoneuronal excitation of three hand muscles determined by a novel pentastimulation technique . Brain . 127 : 1887 - 1898 .
Ziemann U , Ilic TV , Alle H , Meintzschel F. 2004b . Estimated magnitude and interactions of cortico-motoneuronal and Ia afferent input to spinal motoneurones of the human hand . Neurosci Lett . 364 : 48 - 52 .