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1 s2.0 S1053811919304240 Main
NeuroImage
journal homepage: www.elsevier.com/locate/neuroimage
A R T I C L E I N F O A B S T R A C T
Keywords: Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to
Force promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large
EEG vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation
Auditory
of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our
Somatosensory
investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory
Beta oscillations
Cortico-muscular resonance (CMR) stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably,
(ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power.
Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum.
An early, low-frequency region (~4 Hz) reflects the previously-described coupling between the phase-locked EEG
vertex potential and force modulations. A late, higher-frequency region (beta-band, ~20 Hz) reflects a second
coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-
frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the
force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs
across at least two different types of cortical activities, whose functional significance in relation to the motor
system should be investigated further. We propose that these different types of corticomuscular coupling are
important to alter motor behaviour in response to salient environmental events.
1. Introduction events on both electrocortical brain activity and motor output (Novem-
bre et al., 2018). We made two basic observations. First, salient stimuli,
The human brain has evolved to cope with changing environments. regardless of their sensory modality, evoke an involuntary, multiphasic
To do so, appropriate behaviours must be deployed in response to salient modulation of isometric force exertion. This modulation consists of an
sensory events. Thus, sensory and motor systems must cooperate, inter- initial force decrease (~100 ms post stimulus), followed by a force in-
twining the detection of behaviourally-relevant information with the crease (~250 ms), and by another longer lasting force increase (~350 ms
execution of appropriate motor responses (Prinz, 1997; Hommel et al., up to ~2000 ms). Second, we observed that this force modulation is
2001; Ullsperger et al., 2014; Wessel and Aron, 2017). However, sensory tightly coupled with the well-known EEG vertex potential (or vertex
and motor systems are often studied in isolation, and the neurophysio- wave) evoked by salient sensory stimuli (Davis, 1939; Bancaud et al.,
logical consequences of sudden environmental changes are mostly 1953; Mouraux and Iannetti, 2009). We used the term Cortico-Muscular
interpreted from a sensory perspective (Arnal and Giraud, 2012; Jensen Resonance (CMR) to refer to this basic physiological mechanism, which
et al., 2012), ignoring the principle that perception ultimately serves and might subserve the preparation of appropriate behaviour in response to
guides action (Wolpert and Kawato, 1998; Horvitz, 2002). salient stimuli (Novembre et al., 2018).
To fill this gap, we recently explored the effect of unexpected sensory All our previous observations were made in the time domain, and
* Corresponding author. Neuroscience and Behaviour Laboratory, Istituto Italiano di Tecnologia (IIT), Viale Regina Elena, 291, 00161 Roma, Italy.
E-mail address: giacomo.novembre@iit.it (G. Novembre).
https://doi.org/10.1016/j.neuroimage.2019.05.032
Received 16 January 2019; Received in revised form 6 March 2019; Accepted 10 May 2019
Available online 11 May 2019
1053-8119/© 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
G. Novembre et al. NeuroImage 198 (2019) 221–230
therefore might not capture the full coupling between cortical and was previously analysed in the time-domain (Novembre et al., 2018). All
muscular processes elicited by salient stimuli. For this reason, here we time-frequency analyses presented here are novel and have never been
explored both the brain and the force responses in the time-frequency reported before.
domain. We simultaneously recorded EEG and Force while human par-
ticipants were exerting a constant isometric force on a transducer using 2.2. Experimental design
the thumb and the index finger of the right hand, and receiving isolated,
fast-rising, and non-task-relevant somatosensory or auditory stimuli Experiments were conducted in a dim, silent, temperature-controlled
(Fig. 1). room. Participants sat in front of a table, with the ulnar aspect of the
Specifically, we first extensively characterised the modulations of forearm resting on the table surface. They were asked to exert a constant
EEG spectral power (i.e., event-related suppression or enhancement of isometric force on a transducer, which was held between the index finger
power) induced by somatosensory and auditory stimuli, and distin- and thumb of the right hand. While exerting the force, participants
guished phase-locked from non-phase-locked spectral modulations using received either auditory or somatosensory stimuli. In a short preliminary
the Phase Locking Value (PLV; Lachaux et al., 1999). Second, we used the session, participants were familiarised with the stimuli. Participants were
same analytical approach to explore the modulations of Force spectral explicitly told that the stimuli were not task related. The experimental
power induced by the same stimuli. Finally, given that we observed setup is illustrated in Fig. 1.
remarkable similarities between the modulations of EEG and Force The experiment consisted of 14 blocks. Before each block, partici-
power, we explored their coupling by correlating the two spectral powers pants were instructed to keep their eyes closed (to minimize distraction
across trials (“over trials” correlations; Cohen, 2014). This analysis tested and reduce eye movements) and exert a gradually increasing force, until
whether trials with large modulations of EEG oscillatory power also they reached a level comprised between 1 and 2 N. Feedback to the
entailed large modulations of Force oscillatory power at the same latency participants was provided verbally by the experimenters, who could read
and frequency. All analyses were conducted using a fully data-driven the measured force in real time. Once the correct level of force was
approach, i.e. forming significant clusters over time points, frequency reached, participants were instructed to keep the applied force as con-
bins and neighbouring electrodes, corrected for multiple comparisons stant as possible, and the block started.
using a non-parametric cluster-based permutation method (Maris and During each block, participants received 5 to 7 auditory or somato-
Oostenveld, 2007). sensory stimuli at each of three intensities (low, middle, high), as
detailed below. The order of stimulus modality and intensity was ran-
2. Materials and methods domized, and the inter-stimulus interval was 6–10 s (rectangular distri-
bution). Therefore, the average duration of the applied force in one block
2.1. Participants was approximately 48 s. There was a short pause of approximately 5–10 s
between consecutive blocks. During the pauses, participants had to open
Twenty-eight right-handed healthy human participants (14 males, their eyes, and to interrupt the force exertion. Each participant received
mean age [SD] 23.8 3.3 yrs, age range 19–31 yrs) took part in the 14 stimuli for each intensity and modality, for a total of 84 stimuli.
experiment. All participants gave written informed consent and were
paid for their participation. All procedures were approved by the ethics 2.3. Sensory stimuli
committee of University College London. A subset of the current dataset
Auditory stimuli consisted of a fast-rising tone (rise and fall time 5 ms,
frequency 4,000 Hz, duration 50 ms), which was presented through a
single CAT LEB-401 loudspeaker placed in front of the left hand of the
participant. Somatosensory stimuli were constant-current square-wave
electrical pulses (duration 200 μs; Digitimer DS7A) delivered through a
pair of cutaneous electrodes placed over the left median nerve at the
wrist.
Stimuli were delivered at three intensities: low, middle and high.
Stimulus intensity was adjusted individually prior to the beginning of
each experiment. High intensity corresponded to the maximal loudness
(for auditory stimulation) or current (for electrical stimulations) that
each participant could tolerate without feeling discomfort or pain. This
was determined by presenting participants with gradually increasing
stimulus intensities, starting with bearably noticeable stimuli. Partici-
pants were asked whether each stimulus was causing pain or discomfort.
The resulting intensity of the high auditory stimuli never exceeded 70 dB
of sound pressure level, while the intensity of the high electrical stimu-
lations never exceeded 60 mA (average high electrical stimula-
tion ¼ 26.4 mA). Middle and low stimulus intensities were 60% and 20%
of the high stimulus intensity, respectively. All stimuli did not elicit an
overt startle response, as further discussed in our previous work
describing the current procedure (Novembre et al., 2018).
Stimulus presentation was controlled using the software Presentation
(Neurobehavioral systems). Triggers synchronized with stimulus onset
Fig. 1. Experimental protocol (adapted from Fig. 1 of Novembre et al., 2018).
were sent to two computers used for acquiring Force and EEG data.
Participants were instructed to perform an isometric motor task: applying a
constant force on a transducer using the thumb and index finger of the right
hand, while keeping their eyes closed. Meanwhile, we delivered either so- 2.4. Force recording
matosensory stimuli (electrical stimulation of the left median nerve) or acoustic
stimuli (through a loudspeaker placed close to the participant's left hand). All The force applied by the participants (see Experimental Design,
stimuli were isolated, fast-rising and non-task-relevant. The timing of the stimuli above) was sampled using a force-torque (F-T) transducer (ATI nano17,
and their order were randomized. EEG and force were recorded simultaneously. Industrial Automation, calibration ¼ SI-12-0.12, resolution ¼ 3.125 mN).
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This device measures mechanical responses using silicon strain gauges 2.8. Time-frequency analysis of EEG and force timeseries
within a monolithic design to provide high stiffness characteristics whilst
protecting against noise. The device allows recording six components of A time-frequency representation of each EEG and Force epoch was
force and torque (Fx, Fy, Fz, Tx, Ty, Tz). The ‘Fz’ component represented obtained using a windowed Fourier transform with a variable-width
the direction towards which participants were instructed to exert the Hanning window moving in steps of 10 ms. The width of the Hanning
force while holding the transducer (Fig. 1), and it was the source of the window decreased linearly with frequency, from 500 ms (used to esti-
data reported hereafter. The transducer was connected to a data acqui- mate the lowest frequency: 1 Hz) to 100 ms (used to estimate the highest
sition card (National Instruments 6363) through which the sensor data frequency: 40 Hz). These widths are appropriate for identifying both high
from the silicon strain gauges was converted into F-T information based and low frequency responses evoked by salient stimuli while avoiding
upon calibrated values established by the manufacturer. At the start of that estimates of post-stimulus responses are contaminated by pre-
each recording session, the F-T information was set to zero to mitigate the stimulus activity (Zhang et al., 2012; Hu et al., 2015).
effects of potential sensor drifts. Data were sampled at 500 Hz with This analysis yielded, for each single trial, power estimates P(t,f) at
unique timestamps to allow synchronisation with the stimulation trig- each (t,f) bin of the time-frequency plane extending from 1 to þ3 s in
gers. To facilitate two-finger grip, the transducer was mounted in be- the time domain, and from 1 to 40 Hz (in steps of 1 Hz) in the frequency
tween two plastic cylindrical extensions (Fig. 1). domain. The magnitude of the stimulus-induced power changes [PC(f,t)]
was estimated as follows:
2.5. EEG recording PC(t,f) ¼ [P(t,f) – R(f)] /[P(t,f) þ R(f)]
The EEG was recorded using a 32-channel amplifier (SD-LTM-32 Where P(t,f) is the power spectral density at each time-frequency bin
Express, Micromed Italy) at a sampling rate of 1,024 Hz (hardwired high- (t,f), and R(f) is the average power spectral density of the signal enclosed
pass filter ¼ 0.15 Hz), from 26 Ag–AgCl electrodes placed on the scalp within the prestimulus reference interval for each estimated frequency f
according to the International 10–20 system and referenced to the nose. (van Ede et al., 2010, 2011). The range of the prestimulus reference in-
Electrode positions were ‘Fp1', ‘Fpz’, ‘Fp2', ‘F7', ‘F3', ‘Fz’, ‘F4', ‘F8', ‘T3', terval t was proportional to the frequency of interest, and was defined as:
‘C3', ‘Cz’, ‘C4', ‘T4', ‘T5', ‘P3', ‘Pz’, ‘P4', ‘T6', ‘O1', ‘Oz’, ‘O2', ‘FCz’, ‘FC4',
-t1(f) < t(f) < -t2(f)
‘FC3', ‘Cp3', ‘Cp4' (Sharbrough et al., 1991). The electro-oculogram
(EOG) was recorded from two pairs of surface Ag–AgCl electrodes, Where t1 is twice the width of the time window used to estimate power at
with one electrode placed laterally to the outer canthus and the other each frequency f, and t2 is half of the width of the time window used to
below the lower eyelid. Impedances were kept below 10 kΩ. estimate power at each frequency f. The power values within this interval
were averaged to obtain R(f).
2.6. Force data processing The time-frequency representation of induced change in oscillatory
power computed as described above contains both phase-locked and non-
Force magnitude time series were first interpolated to obtain a regular phase-locked responses. To distinguish between phase-locked and non-
sampling rate of 1,000 Hz. Continuous data were band-pass filtered at phase-locked responses, we calculated the phase-locking value (PLV)
0.5–45 Hz (Butterworth, third order) and then segmented into epochs of (Lachaux et al., 1999), which represents a measure of phase consistency
4 s (1 to þ3 s relative to stimulus onset). Trials contaminated by arte- across trials, as follows:
facts (0.3 N from the mean of the pre-stimulus interval) or deviating
1 XN
more than 4 SDs from the participant's mean exerted force across all trials PLVðt; f Þ ¼ eið∅t;f ;r Þ
were excluded from further analyses (this was done separately within N r¼1
each sensory modality and energy). The corresponding EEG trials were
also excluded. These trials constituted 18% of the total number of trials. where N is the number of trials, while ∅ is the phase calculated on each
trial r at the time t and frequency f. Thus, the PLV is 1 if all trials are
perfectly phase-locked at a given time-frequency bin. PLV were finally
2.7. EEG processing
baseline corrected by subtracting the PLV of the prestimulus reference
interval R(f) from each post-stimulus bin, to express stimulus-evoked
Continuous EEG data were first band-pass filtered at 0.5–95 Hz
changes in phase locking: the Phase Locking Change (PLC).
(Butterworth, third order), and then segmented into epochs of 4 s (1 to
þ3 s relative to stimulus onset). A notch filter (47–53 Hz, Butterworth,
third order) was used to reduce data contamination due to power line 2.9. Statistical analysis
noise. All epochs were visually inspected, and those contaminated by
large artefacts due to head movement or muscle contractions were Two sets of statistical analyses were performed. The first treated EEG
excluded from further analyses. The corresponding Force trials were also and Force independently, and aimed to identify significant stimulus-
excluded. These trials constituted 2.0% of the total number of trials. induced changes in the EEG and Force time-frequency spectra. The sec-
Artefacts due to eye blinks or eye movements were subtracted using a ond set of analyses aimed to investigate the relationship between
validated method based on an Independent Component Analysis (Jung stimulus-induced changes in EEG and Force. Specifically, it tested
et al., 2000). In all datasets, independent components related to eye whether trials associated with large EEG power were also associated with
movements had a large EOG channel contribution and a frontal scalp large Force power at the same latency and frequency (correlations “over
distribution. As requested by one of the reviewers, we minimised the trials”) (Cohen, 2014).
possible contribution of eye blinks and eye movements by re-referencing
the EEG data to the average of all peripheral electrodes (i.e. Fp1, Fpz, 2.9.1. Stimulus-induced EEG and force time-frequency modulations
Fp2, F7, F8, T3, T4, T5, T6, O1, Oz, O2). This peripheral average refer- For both EEG and Force data, single-trial time-frequency spectra
ence was preferred to the average reference across all electrodes because belonging to the same experimental modality (i.e., somatosensory or
(1) we only recorded from 26 electrodes, and (2) these electrodes were auditory) were averaged together, thus yielding two PC(t,f) spectra for
unevenly distributed across the scalp, with a higher electrode density each participant.
over the scalp vertex (i.e. where the largest part of the stimulus-evoked To assess the consistency of stimulus-induced spectral modulations
response is recorded). To match the sampling rate of the force times- across participants, these averages were entered into a non-parametric
eries, EEG epochs were finally downsampled to 1,000 Hz. cluster-based permutation testing (Maris and Oostenveld, 2007), which
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consisted of two steps. First, the values of each PC(t,f) bin were con- PC(t,f) power spectra was analysed at the trial-by-trial level. With this
trasted against zero (i.e. against baseline), using one-sample t tests. Next, analysis we tested whether the trial-by-trial variability in EEG power was
bins significantly different from zero (p < 0.05) were clustered together if related to the trial-by-trial variability of Force power. To achieve this,
they were consecutive either in time or in frequency. When this analysis each EEG and Force time-frequency bin was smoothed over time using a
was conducted on the EEG data, clusters were also based on the spatial sliding window of 10 time bins (corresponding to 100 ms). Next, for each
adjacency of the EEG channels. Specifically, a cluster had to be composed time-frequency bin, we calculated a trial-by-trial correlation coefficient
of at least two neighbouring (t,f) bins (either in time or in frequency) (Spearman's rs) between EEG and Force. This yielded, for each participant
with a p value < 0.05 on at least three neighbouring EEG channels. When and EEG electrode, a time-frequency correlation matrix consisting of
this analysis was conducted on the Force data, for which we had only one 240 40 (time x frequency) Spearman's rs values (the total window time
channel, only consecutivity in time domain or adjacency in the frequency range was 0.4–2 s). Finally, these Spearman's rs values were Fisher's z-
domain were considered. transformed.
Once the clusters were identified, a significance test statistic of each The across-participants consistency of over trials correlation matrices
cluster was computed by summing the t values of the bins composing it. was assessed by using the same non parametric cluster-based permuta-
Next, to assess the significance of each cluster, we used permutation tion test discussed above (see Stimulus-induced EEG and Force time-
testing against 0 (i.e. against baseline), to generate a random significance frequency modulations), here contrasting the correlation coefficients vs.
distribution (1000 permutations). This random distribution was used to zero. Thus, resulting positive clusters would index significant positive
define a threshold (p ¼ 0.05) against which the actual significant clusters correlations between EEG and Force power, while negative clusters
were assessed. would index negative correlations.
The phase locking change PLC(t,f) were analysed following the same
procedure described above.
2.9.3. Test of lateralization (TOL)
2.9.2. Relationship between EEG and force time-frequency power
Correlations over trials. The relationship between EEG and Force When statistical analyses yielded significant clusters of stimulus-
induced power changes (PC) or EEG-Force correlations (rs), we tested
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whether their scalp distribution was lateralised, using the following oscillations (α-suppression; cluster C: ~0.5–1.9 s, ~8–10 Hz). In addi-
procedure. We first averaged the PC or rs values separately for the left tion, only somatosensory stimuli induced an additional transient sup-
electrodes Cp3, C3 and FC3, and for the right electrodes Cp4, C4 and FC4, pression of beta-band oscillations (β-suppression; cluster D: ~0.2–0.3 s,
in each participant. The two resulting values were compared across ~15–30 Hz).
participants using a paired-sample t-test. Negative t-values implied a The power increases A1 and A2 were modulations of low (1–10 Hz,
lateralization towards the left hemisphere, while positive t-values 0–0.9 s) and high (10–40 Hz, 0–0.2 s) frequencies, respectively (Fig. 3,
implied a lateralization towards the right hemisphere. This test of cluster-corrected significance: p < 0.001 [somatosensory stimulus],
lateralization is below referred to as TOL. p < 0.001 [auditory stimulus]). The sub-cluster A1 is largely concomitant
to the biphasic vertex potential observable in the time domain (Fig. 2,
3. Results upper plots, PLC cluster-corrected significance: p < 0.001 [somatosen-
sory stimulus], p < 0.001 [auditory stimulus]). Several previous reports
Fig. 2 shows the results of the phase-locking change (PLC) analysis, have indeed demonstrated that this power increase is the time-frequency
which isolates phase-locked modulations of spectral power. Fig. 3 instead representation of the (transient) phase-locked biphasic vertex potential
shows both phase-locked and non-phase-locked modulations of spectral observed in the time domain (Mouraux et al., 2003; Hu et al., 2014). In
power. Thus, modulations displayed in Fig. 3 but not in Fig. 2 are non- support of this interpretation, we noticed (i) that the PLC analysis showed
phase-locked. In the following sections, we mainly describe the results that these responses are clearly phase-locked (Fig. 2), and (ii) that the
displayed in Fig. 3, which comprises all modulations. We sporadically ERP time-frequency response and the vertex potential in the time domain
refer to Fig. 2 when discussing phase-locked modulations. have extremely similar scalp topographies (Fig. 2, upper plots). Instead,
the second sub-cluster (A2) has a frontal and more widespread topog-
raphy (Fig. 2). Therefore, A2 is a time-frequency response potentially
3.1. Stimulus-induced modulations of EEG spectral power reflecting a mixture of activities, likely entailing both early- and
middle-latency phase-locked brain potentials (peaking up to 60 ms
The upper panels of Fig. 3 display the stimulus-induced modulations post-stimulus, for a review see (Cruccu et al., 2008; Pratt, 2012)) and
of EEG spectral power at electrode Cz, together with their cross- minute non-phase-locked micro-saccades induced by the salient stimuli
participants consistency and the corresponding scalp topographies (the possible contribution of micro-saccades is suggested by the frontal
(Fig. 3, upper panels). Both somatosensory and auditory stimuli elicited distribution shown in Fig. 3).
three significant modulations. These consisted of one phase-locked Both somatosensory and auditory stimuli elicited a long-lasting
response, largely corresponding to the ERP observable in the time- β-enhancement (Fig. 3, cluster B; cluster-corrected significance:
domain (ERP, composed of two subclusters previously described as p < 0.001 [somatosensory], p 0.001 [auditory]), which was strongest
separate responses: A1: 0–0.9 s, 1–10 Hz, and A2: 0–0.2 s, 10–40 Hz; over the central electrodes of the scalp, without a consistent lateraliza-
Mouraux et al., 2003; Iannetti et al., 2008), and two non-phase-locked tion across sensory modalities (TOL: t ¼ 0.97 p ¼ 0.33 [somatosensory],
responses: (i) an enhancement of beta-band oscillations (β-enhancement; TOL: t ¼ 1.40 p ¼ 0.17 [auditory]).
cluster B: 0.5–1.5 s, ~13–30 Hz), and (ii) a suppression of alpha-band
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Both somatosensory and auditory stimuli also elicited a α-suppression 3.3. Relationship between EEG and force modulations
(Fig. 3, cluster C: cluster-corrected significance: p ¼ 0.0571 [somatosen-
sory], p ¼ 0.012 [auditory]). The scalp distribution of this α-suppression Over-trials correlations. This analysis explored the correlation between
was different in the two modalities: following somatosensory stimuli it the trial-by-trial variability of EEG and Force power spectra: it explored
was slightly stronger on the central-parietal electrodes, while following whether trials associated with large EEG power also had large Force
auditory stimuli it was maximal on the midline, without clear evidence of power at the same latency and frequency. There were two significant
lateralization (TOL: t ¼ 0.72, p ¼ 0.78 [somatosensory], TOL: t ¼ 0.75 clusters showing positive trial-by-trial correlations.
p ¼ 0.45 [auditory]). The first cluster (~0–0.3 s and 3–5 Hz; cluster A, Fig. 4, lower panels;
Only somatosensory stimuli induced an additional decrease of β cluster-corrected significance: p < 0.001 [somatosensory], p ¼ 0.02
power, i.e. a β-suppression (Fig. 3, cluster D; cluster-corrected signifi- [auditory]) reflected the previously described correlation between the
cance: p ¼ 0.024). This β-suppression occurred between 0.2 and 0.3 s, just negative and positive VW in the time domain, and the first force increase
before the β-enhancement. Its scalp distribution was widespread over of the CMR (Novembre et al., 2018). These correlations are reminiscent
central-parietal electrodes and not lateralised (TOL: t ¼ 1.12, p ¼ 0.26). of the lateralised distributions of the correlation between the positive VW
and the force increases that we previously observed in the time domain,
3.2. Stimulus-induced modulation of force spectral power and are further discussed below (topographies A-D in Fig. 5 of Novembre
et al., 2018) (TOL: t ¼ 0.21, p ¼ 0.83 [somatosensory], t ¼ 2.07,
The time-frequency analysis of Force timecourses revealed that both p ¼ 0.047 [auditory]).
somatosensory and auditory stimuli elicited three significant modula- The second cluster (~0.3–1.5 s [somatosensory], ~0.75–1.5 s [audi-
tions of power (Fig. 3, bottom panels). These consisted of a (i) phase- tory], and 15–28 Hz; cluster B, Fig. 4, lower panels; cluster-corrected
locked power increase at ~0–0.5 s and 2–15 Hz (Fig. 3, bottom panel, significance: p < 0.001 [somatosensory], p ¼ 0.008 [auditory]) re-
cluster 1), (ii) a non-phase-locked power increase at ~0.5–1.5 s and flected the trial-by-trial correlation between the stimulus-induced non-
13–30 Hz (Fig. 3, bottom panel, cluster 2), and (iii) a non-phase-locked phase-locked β-enhancement in the EEG (Fig. 3, cluster B, top panel) and
power decrease at ~0.75–2 s and 1–5 Hz (Fig. 3, bottom panel, cluster 3). the concurrent and isofrequent power increase in the force (Fig. 3, cluster
The first power increase (Fig. 3, cluster 1; 0–0.5 s and 2–15 Hz; 2, bottom panel). Thus, trials with large β-enhancement also had large
cluster-corrected significance: p < 0.001 [somatosensory], p < 0.001 power in force oscillations at the same latency and frequency. In both the
[auditory]) reflects the first two (transient) modulations composing the auditory and somatosensory modality, this second cluster of correlations
CMR observed in the time-domain and phase-locked to the stimulus onset was clearly lateralised, and strongest on the electrodes overlying the
(Novembre et al., 2018): the initial force decrease peaking at ~100 ms hemisphere contralateral to the hand exerting the force (topographies B
post stimulus, and the following force increase peaking at ~250 ms post in bottom panels of Fig. 4) (TOL: t ¼ 3.30, p ¼ 0.002 [somatosensory],
stimulus (Fig. 2, bottom panels). This interpretation is confirmed by the t ¼ 3.65, p ¼ 0.001 [auditory]).
PLC analysis, which showed that this power modulation was clearly
phase-locked (Figs. 2 and 3). 4. Discussion
The power decrease (Fig. 3, cluster 3; ~0.75–2 s and 1–5 Hz; cluster-
corrected significance: p ¼ 0.017 [somatosensory], p ¼ 0.007 [auditory]) We characterised the modulations of electrocortical (EEG) and
reflects the second (‘late’) increase of isometric force in the CMR detected muscular (Force) spectral power induced by salient environmental
in the time domain. This late force increase in the time domain is more stimuli, as well as the relationship across trials between such modula-
visible after prestimulus detrending (Novembre et al., 2018), as shown in tions. We report two main results. First, somatosensory and auditory
the gray waveform of Fig. 2. When the waveform is not detrended and the stimuli elicited similar modulations of spectral power in both EEG and
timecourse is transformed in the time-frequency domain, the late force Force measures. In each measure, modulations were both phase-locked
increase appears as a decrease in power. This occurs because the baseline and non-phase-locked. Second, we identified two time-frequency re-
force signal is characterised by an ongoing negative “proprioceptive” gions where stimulus-induced EEG and Force modulations were coupled.
drift (highlighted with an arrow in Fig. 2), reflecting the well-known One region corresponded to the phase-locked modulations that have
decrease of exerted force throughout a holding task, a physiological been already demonstrated to be coupled in the time domain (Novembre
phenomenon likely due to a gradual reduction of proprioceptive sensi- et al., 2018). The second region corresponded to the non-phase-locked
tivity (Wann and Ibrahim, 1992; Wolpert et al., 1998; Desmurget et al., increase of power observed both in the EEG and in the Force at
2000; Nazir et al., 2017). Given that the ongoing proprioceptive drift is approximately 20 Hz, and ~0.5–1.5 s post-stimulus. These results show
reduced by the stimulus, after baseline correction a decrease of power at that sudden environmental stimuli lead to a strong coupling between
what is likely the frequency of the prestimulus drift appears. cortical activity and exerted force not only in phase-locked responses but
Interestingly, the time-frequency analysis of the force timecourse also also in β-band, non-phase-locked cortical oscillations. Thus,
disclosed a modulation that did not simply reflect the time-frequency stimulus-induced corticomuscular coupling occurs across at least two
counterpart of the CMR observed in the time domain. Indeed, both so- different types of cortical activities.
matosensory and auditory stimuli induced a second power increase
(Fig. 3, cluster 2; 0.5–1.5 s and 13–30 Hz; cluster-corrected significance: 4.1. Supramodal modulation of EEG spectral power
p < 0.001 [somatosensory], p < 0.001 [auditory]). Since this modulation
was not phase-locked, as shown by the PLC analysis (Fig. 2), it was not Somatosensory and auditory stimuli elicited similar patterns of EEG
visible after across-trial averaging in the time domain. This modulation of activity. These patterns consisted of both phase-locked and non-phase-
power had a time-frequency distribution remarkably similar to the locked (Figs. 2 and 3) modulations of spectral power.
β-enhancement observed in the EEG data (cluster ‘B’ in the upper panels of Phase-locked ERP. The stimulus-induced phase-locked response (ERP,
Fig. 3), raising the intriguing possibility that the two phenomena are sub-cluster A1) entailed a short latency (0–0.9 s) power increase of low
related to one another. This possibility was explored in the analysis of the (1–10 Hz) frequencies. This phase-locked modulation is the time-
relationship between the Force and the EEG power spectra. frequency representation of the biphasic EEG vertex potentials detected
at the same latency in the time domain (Davis, 1939; Bancaud et al.,
1953; Carmon et al., 1976; Naatanen and Picton, 1987). Several previous
1
We report this result as the cluster-based permutation test used to detect it is reports have indeed demonstrated that the vertex potential can be eli-
very conservative. Moreover, we highlight that this response has been observed cited by sudden stimuli of distinct modalities (Mouraux and Iannetti,
in other studies, as detailed in the Discussion. 2009; Liang et al., 2010; Valentini et al., 2011), and that such potential
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has a time-frequency representation similar to the one we observed here movement termination (Pfurtscheller and Lopes Da Silva, 1999). More
(Mouraux et al., 2003; Mouraux and Iannetti, 2008; Hu et al., 2014, importantly with respect to our current results, β oscillations increase
2015; Hu and Iannetti, 2019). In support of this view, the scalp distri- while holding a posture (Gilbertson et al., 2005), and, as further dis-
bution of the ERP cluster was centrally distributed and strongest over the cussed in the next paragraph, can even be recorded directly from the
vertex (Figs. 2 and 3), like the vertex potential in the time domain muscles involved in the motor task using EMG (Baker et al., 1997; Kilner
(Fig. 2). et al., 1999). Thus, considering that our participants had to exert an
Non-phase-locked α-suppression and β-suppression. The stimuli also eli- isometric force (Fig. 1), both the somatosensory and the
cited non-phase-locked decreases of spectral power: an α-suppression auditory-induced β-enhancement that we observed likely reflect the
induced by both the somatosensory and the auditory stimuli, and a impact of salient environmental stimuli on the ongoing dynamics of the
β-suppression only induced by somatosensory stimuli (Fig. 3). These non- motor system.
phase-locked suppressions have been repeatedly reported. Both α- and
β-suppressions are elicited by somatosensory stimuli, with a maximum 4.2. Supramodal modulation of force spectral power
above the primary sensorimotor cortex2 (Salenius et al., 1997a,b; Cheyne
et al., 2003; Bauer et al., 2006; van Ede et al., 2011). In contrast, auditory Somatosensory and auditory stimuli elicited virtually identical spec-
stimuli have been shown to elicit only α-suppression, which is commonly tral modulations of Force. They consisted of one phase-locked and two
described as having a central distribution consequent to activity localized non-phase-locked responses (Figs. 2 and 3).
in the bilateral auditory cortex (like in the current results, Fig. 3) (Lehtela The previously-described first two CMR components in the time
et al., 1997; Weisz et al., 2011; Hartmann et al., 2012; Obleser and Weisz, domain (Novembre et al., 2018) fully explain the current observation of a
2012). From a functional perspective, both α- and β-suppressions have phase-locked modulation of spectral power occurring in the 500 ms
been associated with perceptual and attentional processes, with stronger following the stimulus, and divided in two subclusters: one with a
suppression associated with better auditory and somatosensory time-frequency maximum at 0.1 s and ~15 Hz, reflecting the first force
discrimination (Foxe and Snyder, 2011; van Ede et al., 2011; Obleser and decrease in the time domain (subcluster ‘1B’ in Fig. 2), and one with a
Weisz, 2012). time-frequency maximum at 0.25 s and ~4 Hz, reflecting the following
Non-phase-locked β-enhancement. The most interesting time-frequency force increase in the time domain (subcluster ‘1A’ in Fig. 2). In contrast,
EEG response was the non-phase-locked β-enhancement, which was eli- the last more sustained CMR component explains the low-frequency
cited by both somatosensory and auditory stimuli (Fig. 3). This non-phase-locked modulation of spectral power observed from ~0.75 s
β-enhancement is commonly observed following somatosensory stimuli, following the stimulus (cluster ‘3’ in Fig. 3).
and, in this modality, it is often described as a “rebound” because it More remarkably, the time-frequency analysis revealed an additional
typically follows a preceding β-suppression (described in the previous non-phase-locked increase of spectral power in a time-frequency region
paragraph) (Salmelin and Hari, 1994; Cheyne et al., 2003; Bauer et al., similar to the one containing the cortical β-enhancement (clusters ‘B’ and
2006). Its scalp distribution is central, and usually stronger over the ‘2’ in Fig. 3). This spectral modulation, occurring at 0.5–1.5 s with a
hemisphere contralateral to the stimulated limb (Neuper and Pfurtsch- mean frequency of ~20 Hz, was elicited by both auditory and somato-
eller, 2001; Pfurtscheller et al., 2001; Neuper et al., 2006). The sensory stimuli. Importantly, this modulation cannot be directly
β-enhancement is usually not observed in response to auditory stimuli (but explained by any of the CMR components observed in the time domain as
see (Leventhal et al., 2012)), unless participants have to perform a task it was non-phase-locked, and therefore not detectable by the phase
entailing an association between the auditory stimulus and movements locking change (PLC, Fig. 2). Both increases and decreases of oscillatory
or actions (Caetano et al., 2007; Fujioka et al., 2012). This is not sur- activity in frequencies overlapping with the cortical β (13–30 Hz) have
prising, given that β oscillations have been repeatedly shown to be been identified in the EMG during a number of sensorimotor tasks (Baker
associated with motor functions (Pogosyan et al., 2009; Novembre et al., et al., 1997; Kilner et al., 1999; van Ede and Maris, 2013). Such EMG
2017). For instance, β oscillations originating from somatosensory activity has been shown to result in an actual finger “microtremor” at the
cortices typically decrease during movement, and rebound following same frequency, which can be detected by isometric force transducers
(McAuley et al., 1997; Gilbertson et al., 2005; Airaksinen et al., 2015). It
must be noted that these earlier observations of oscillatory activity of
2 both EMG and force at ~20 Hz were made in studies entailing purely
Note that this should not be taken as direct evidence that this signal is
generated in the primary somatosensory cortex. motor tasks. Here not only we confirm the existence of such 20 Hz
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activities, but we also show that they are enhanced by environmental β-band might reflect the nervous system's attempt to achieve motor sta-
salient stimuli. To better understand the functional significance of these bility following the force perturbation reflected by the first two compo-
oscillations, we need to consider their relationship with the concomitant nents of the CMR, on the basis of a transient change in proprioceptive
stimulus-induced cortical activity. afference. From this perspective, the β-band coupling would be caused
by, and therefore be part of, the CMR itself. In line with this reasoning,
4.3. Coupling of EEG and force spectral modulations another study showed that auditory and visual distractors transiently
modulate isometric force,3 and that this modulation is followed by a
To explore the relationship between EEG and Force spectral modu- longer-lasting increase of MEG-EMG β-band coupling, which was inter-
lations, we correlated the power of the two measures over trials. This preted as a recalibration of the ongoing (tonic) corticospinal coupling
analysis tested whether trials with large modulations of cortical oscilla- (Piitulainen et al., 2015).
tory power also entailed large modulations of Force oscillatory power at Alternatively, it is possible that the β-band coupling is caused directly
the same latency and frequency. These results indicated that, following by the stimuli, independently of the earlier components of the CMR. This
both somatosensory and auditory stimuli, EEG and Force signals became interpretation is in agreement with the observation of a clear
coupled in two separate regions of the power spectra. β-enhancement in motor tasks that rely on sensory stimulation, such as the
The first coupled time-frequency region was maximal at ~4 Hz and maintenance or revision of motor plans on the basis of sensory infor-
~0.25 s (Fig. 4). This result is the time-frequency representation of our mation (Tan et al., 2016), or the sudden interruptions of on-going
previous observation that EEG vertex potentials and Force are coupled in behaviour in response to unexpected or infrequent events (Swann
the time domain. More precisely, the coupling we observed in the time- et al., 2009; Ray et al., 2012; Fischer et al., 2016; Wessel et al., 2016;
frequency domain reflects the trial-by-trial correlation between the Wagner et al., 2018; Muralidharan et al., 2019).
amplitude of the P vertex potential and the first force increase elicited by Obviously, future research is needed to understand better the func-
somatosensory stimuli (Fig. 5 in Novembre et al., 2018). The current tional significance of these corticomuscular couplings. This should be
results additionally show that the same trial-by-trial EEG-Force rela- done bearing in mind that these couplings, traditionally observed during
tionship also holds when the cortical and CMR responses are elicited by purely motor tasks (Conway et al., 1995; Baker et al., 1997; Salenius
auditory stimuli (Fig. 4). The topography of this correlation was centrally et al., 1997a,b; McAuley et al., 1997; Mima and Hallett, 1999; Gross
distributed over the electrodes covering sensorimotor regions, and, et al., 2000, 2002; Kristeva-Feige et al., 2002; Jerbi et al., 2007; Air-
following the auditory stimuli, was stronger in the hemisphere contra- aksinen et al., 2015; Ushiyama et al., 2017; Bourguignon et al., 2017),
lateral to the hand exerting the force task. Although the time-frequency can in fact be enhanced by salient sensory stimuli (Piitulainen et al.,
EEG response at ~4 Hz lumps together the N and the P waves of the 2015; Novembre et al., 2018). Thus, to understand these neurophysio-
vertex potential (whose correlations with the force signal in the time logical phenomena, it is important to consider the functional continuum
domain have meaningfully different scalp distribution, see Fig. 5 in between sensory and motor systems.
Novembre et al., 2018), these time-frequency observations are consistent
with an effect of salient sensory stimuli on a number of motor behaviours Conflicts of interest
(Fautrelle et al., 2010; Perfiliev et al., 2010; Pruszynski et al., 2010, 2016;
Pruszynski, 2014; Wood et al., 2015; Moayedi et al., 2015; Gu et al. 2016, The authors declare no conflict of interest.
2017; Scott, 2016; Kilintari et al., 2018; Reuter, 2018). These results are
also consistent with the notion that the vertex potential is elicited by a Acknowledgements
network of cortical regions comprising the anterior cingulate (Mouraux
and Iannetti, 2009, 2018), which is known to be associated with motor This study was funded by The Wellcome Trust (COLL JLARAXR to
control (Shackman et al., 2011; Caruana et al., 2018) via direct pro- GDI), the European Research Council (Consolidator grant PAINSTRAT to
jections to the primary motor cortex and even spinal motor neurons GDI), and an 8 Great Technologies Capital grant (EP/K005030/1).
(Dum and Strick, 1991, 2002).
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