J Neurophysiol 111: 2634 –2643, 2014.
First published March 19, 2014; doi:10.1152/jn.00511.2013.
Localizing evoked cortical activity associated with balance reactions: does the
anterior cingulate play a role?
Amanda Marlin,1 George Mochizuki,2,3 William R. Staines,1,2 and William E. McIlroy1,2
1
Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada; 2Heart and Stroke Foundation, Canadian
Partnership for Stroke Recovery, Sunnybrook Research Institute, Toronto, Ontario, Canada; and 3Department of Physical
Therapy, University of Toronto, Toronto, Ontario, Canada
Submitted 7 August 2013; accepted in final form 17 March 2014
balance; electroencephalography; event-related potentials; reactive
control
LITERATURE HIGHLIGHTS A POTENTIALLY important role for the
cerebral cortex in the control of upright balance in humans
(Ackermann et al. 1986; Jacobs and Horak 2007; Maki and
McIlroy 2007; Ouchi et al. 1999). Indirect evidence comes
from studies that employ dual task paradigms (McIlroy et al.
1999; Norrie et al. 2002), which have revealed a link to
executive function, indicating that cognition and attention
influence balance control (Rankin et al. 2000; Teasdale and
Simoneau 2001). In addition, animal studies have demonstrated evidence of cortical cell discharge linked to evoked
balance reactions (i.e., corrective postural responses to a destabilizing event) (Beloozerova et al. 2003, 2005; Deliagina et
Address for reprint requests and other correspondence: W. E. McIlroy, Dept.
of Kinesiology, Univ. of Waterloo, 200 Univ. Ave, Waterloo, Ontario, Canada
N2L 3G1 (e-mail: [email protected]).
2634
al. 2008; Matsuyama and Drew 2000). The direct evidence
comes from electrophysiological studies with humans that have
revealed a link between the cerebral cortex and the control of
compensatory balance reactions (Adkin et al. 2006; Dietz et al.
1984, 1985; Dimitrov et al. 1996; Duckrow et al. 1999; Jacobs
and Horak 2007; Mochizuki et al. 2008, 2009b, 2010; Quant et
al. 2004a,b; Quintern et al. 1985; Staines et al. 2001).
To date, event-related potential (ERP) studies using electroencephalography (EEG) have revealed two main corticalevoked potentials in response to applied disturbances to balance (e.g., external perturbations). There is an initial small
positivity, the P1 response, representing the earliest nonspecific
response to instability (Dietz et al. 1984), followed by a more
significant and consistently evoked negativity, the N1 response. The peak of the N1 response occurs ⬃100 –150 ms
after the perturbation onset in the fronto-central region of the
brain (Dietz et al. 1984, 1985; Dimitrov et al. 1996; Duckrow
et al. 1999; Quant et al. 2004a,b; Staines et al. 2001). The N1
response has large amplitude, ranging from 10 to 60 ␮V. The
amplitude of the N1 response is variable since it is scaled to the
amplitude of the perturbation. The amplitude of the N1 response appears to be importantly influenced by both the size
(Staines et al. 2001) and predictability of the timing of the
perturbation (Adkin et al. 2006; Jacobs and Horak 2007;
Mochizuki et al. 2008), as well as a concurrent cognitive task
(Quant et al. 2004a) and a concurrent peripheral stimulus
(Staines et al. 2001). In addition, the N1 is a robust response
that is measurable across a range of balance and perturbation
conditions. For example, the N1 has been evoked in association
with compensatory reactions following perturbations in various
postures including sitting (Mochizuki et al. 2009a; Staines et
al. 2001), standing (Adkin et al. 2006; Dietz et al. 1985;
Mochizuki et al. 2008, 2009a, 2010), and walking (Dietz et al.
1985; Quintern et al. 1985). The N1 is also comparable across
different types of tasks including an inverted pendulum tilt
beneath the ankle during sitting (Quant et al. 2004b), chair tilt
(Mochizuki et al. 2009a), platform translation in sitting
(Staines et al. 2001), standing (Dietz et al. 1984, 1985),
walking (Dietz et al. 1984; Quintern et al. 1985), horizontal
perturbations to the trunk in standing (Adkin et al. 2006), and
standing lean and release (Mochizuki et al. 2009a, 2010).
There does remain debate about the potential role of the N1
response, specifically whether it is linked to generic events
such as error detection or whether it is linked to the planning
and execution of ongoing motor responses. Quant et al.
(2004b) suggested that the N1 was not linked to the execution
and planning of motor responses in their ankle pendulum
0022-3077/14 Copyright © 2014 the American Physiological Society
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Marlin A, Mochizuki G, Staines WR, McIlroy WE. Localizing
evoked cortical activity associated with balance reactions: does the
anterior cingulate play a role? J Neurophysiol 111: 2634 –2643, 2014.
First published March 19, 2014; doi:10.1152/jn.00511.2013.—The
ability to correct balance disturbances is essential for the maintenance
of upright stability. Although information about how the central
nervous system controls balance reactions in humans remains limited,
recent literature highlights a potentially important role for the cerebral
cortex. The objective of this study was to determine the neural source
of the well-reported balance-evoked N1 response. It was hypothesized
that the N1 is associated with an “error-detection” event in response
to the induced perturbation and therefore may be associated with
activity within the anterior cingulate cortex (ACC). The localized
source of the N1 evoked by perturbations to standing balance was
compared, within each participant, to the location of an error-related
negativity (ERN) known to occur within the ACC while performing a
flanker task. In contrast to the main hypotheses, the results revealed
that the location of the N1 was not within the ACC. The mean
Talairach coordinates for the ERN were (6.47, ⫺4.41, 41.17) mm,
corresponding to the cingulate gyrus [Brodmann area (BA) 24], as
expected. However, coordinates for the N1 dipole were (5.74,
⫺11.81, 53.73) mm, corresponding to the medial frontal gyrus (BA
6), specifically the supplementary motor area. This may suggest the
N1 is linked to the planning and execution of elements of the evoked
balance reactions rather than being associated with error or event
detection. Alternatively, it is possible that the N1 is associated with
variation in the cortical representation due to task-specific differences
in the activation of a distributed network of error-related processing.
Subsequent work should focus on disentangling these two possible
explanations as they relate to the cortical processing linked to reactive
balance control.
CORTICAL ACTIVITY AND BALANCE REACTIONS
cal processes that may be related to the specific control of the
evoked balance reactions. An important characteristic of the
ERN is the dipole location within the ACC, as it appears to
distinguish a class of cortical activity linked to error detection/
conflict resolution. Therefore, if the N1 response were linked to
error detection, one would hypothesize that the source generator would be in the ACC, paralleling the location of the ERN.
Rather than simply measuring the location of the evoked N1
response, we currently conducted within-subject comparison of
the source location of the N1 to the source location of the ERN
evoked during the performance of a standard flanker task. In
this way, the source localization of the ERN (presumed to
be the ACC) was used as a person-specific reference for
localization of perturbation evoked N1 responses. It was hypothesized that the source location of the perturbation evoked
N1 would be located within the ACC, consistent with the
location of the ERN measured during performance of errors in
the flanker task. The findings from this study would continue to
guide our understanding of the specific role that the cortex
plays in the control of human upright balance.
METHODS
Participants
Eleven healthy young adults (8 females and 3 males, average age
of 26.8 ⫾ 4.5 yr) provided informed consent to participate in this
study. Participants were asked to complete a brief questionnaire about
their medical history indicating that they were free of neurological and
musculoskeletal conditions that could have impacted task performance. This study received approval through the Office of Research
Ethics at the University of Waterloo.
Experimental Protocol
Each participant completed two task conditions: 1) standing lean
and release task to evoke balance reactions and the N1 response, and
2) flanker task to evoke errors and the ERN. The task order was
counterbalanced across participants.
Balance task. Perturbations to standing balance were achieved
using a custom made lean and release cable system that reliably
evokes compensatory balance reactions (Mochizuki et al. 2010). The
participants stood on a force plate in a standardized foot position
(McIlroy and Maki 1997). Participants leaned forward against a
horizontal cable at such an angle so as to maintain a load of 5–7% of
body weight on the cable. The experimenter applied the perturbation
by unpredictably releasing the cable causing the participant to fall in
a forward direction, evoking a compensatory reaction. The magnitude
of the perturbation, determined by the standardized lean angle, was
only large enough to evoke a feet-in-place reaction to recover balance
(i.e., no stepping or grasping). The timing of the perturbations was
randomized; varying from 1 to 15 s once the participant was relaxed
in the forward lean position. A total of 40 trials were collected per
participant.
Flanker task. The participants also performed a speeded modified
flanker task to evoke the ERN. The flanker task used in the present
study is based on the parameters used by Ullsperger and von Cramon
(2001). The participants were instructed to respond as fast and as
accurately as possible to the direction of a target arrow that was
presented briefly on the center of a computer screen with either a left
or right computer mouse button press. All responses were performed
with the right hand. Each participant performed 5- to 10-min blocks to
achieve an adequate number of error trials for ERP analysis. In total,
⬃300 responses were collected, where 50% were presented congruently (i.e., flanker arrows and target arrow were pointing in the same
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study. It has also been suggested that the N1 response represents sensory processing of the perturbation (Dietz et al. 1984;
Quant et al. 2004b). In contrast, Mochizuki et al. (2008, 2010)
demonstrated that the amplitude of the N1 response is strongly
influenced by temporal predictability of the perturbation, independent of the evoked sensory discharge linked to the perturbation. Therefore, rather than a motor or sensory linked response, it has been proposed that the N1 response is more
likely an error signal, reflecting a comparison between the
anticipated central state and the actual state as a result of the
balance disturbance (i.e., error in stability) (Adkin et al. 2006;
Dimitrov et al. 1996). The error detection role, suggesting a
relationship between the evoked negativity and errors in stability, draws parallels to a negativity evoked in other behavioral paradigms: the error-related negativity (ERN) (Pailing
and Segalowitz 2004; Yasuda et al. 2004). Indirect support
comes from the fronto-central topographic representation of
the perturbation-evoked N1 response (Mochizuki et al. 2010;
Quant et al. 2004b), which parallels the topographic distribution of the ERN that occurs after the execution of an erroneous
response in a cognitive task (Falkenstein et al. 1990; Gehring
et al. 1990, 1993; Gemba et al. 1986; Miltner et al. 2003;
Sasaki and Gemba 1986). Since the ERN is only seen in error
trials, it is speculated that it is related to a general error
detection mechanism that monitors and compares a representation of the intended correct response to a representation of the
actual response (Bernstein et al. 1995; Coles et al. 2000;
Dehaene et al. 1994; Falkenstein et al. 2000; Gehring et al.
1993; Miltner et al. 2003; Scheffers and Coles 2000; Ullsperger and von Cramon 2001). It is noteworthy that there is
evidence that this ERN may well reflect a more generic process
common to event novelty as well as error processing (Wessel
et al. 2012). The question that follows is whether the N1
evoked by postural instability is a reflection of a generic error
detection mechanism with activity linked to the anterior cingulate cortex (ACC) as proposed by Adkin et al. (2006).
We proposed that the source location of the N1 response
might provide some insight into the potential role of this
evoked cortical activity. The association between the N1
evoked by balance perturbations and the ERN evoked in
error-detection tasks may be indirectly revealed by the relationship of their corresponding dipole locations. Error processing has been shown to involve a network of brain regions,
including the supplementary motor area (SMA), insula, parietal
cortex, thalamus, and cerebellum (Gallea et al. 2008; Harsay et
al. 2012; Huster et al. 2011; Ide and Li 2011; Reinhart et al.
2012; Stemmer et al. 2004). Importantly, neurophysiological
studies in monkeys (e.g., Gemba et al. 1986; Niki and Watanabe 1979; Shima and Tanji 1998), functional MRI studies in
humans (e.g., Carter et al. 1998, 2001; Kerns et al. 2004; Kiehl
et al. 2000; Menon et al. 2001; Ullsperger and von Cramon
2003), as well as dipole source localization studies in humans
(e.g., Badgaiyan and Posner 1998; Dehaene et al. 1994; Holroyd et al. 1998; Miltner et al. 1997, 2003), implicate the ACC
as being a key brain region in error processing.
The objective of the current study was to determine whether
the N1 response, evoked during balance control, reflects cortical processing linked to activity of the ACC, thus reflecting
error detection and/or conflict monitoring. Under such a model,
one would argue that the evoked N1 response is a generic
response to the “perturbation event” rather than specific corti-
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CORTICAL ACTIVITY AND BALANCE REACTIONS
direction) and the other 50% were presented incongruently (i.e.,
flanker arrows and target arrow were pointing in opposite directions).
The congruent and incongruent trials were randomized over the
10-min block. The participants were given a 1- to 2-min break
between blocks to minimize fatigue.
Data Acquisition
Data Analysis
Electroencephalography. Postprocessing for the EEG data was
done in Neuroscan 4.3. The same analysis steps were utilized for both
task conditions. Epochs were response locked to the onset of the
perturbation (balance task) or button press (flanker task). Each epoch
was low-pass filtered at 30 Hz and baseline corrected using the
average amplitude of the first 100 ms of that epoch (i.e., ⫺600 to
⫺500 ms). Each epoch was then visually scanned for ocular artifact
and epochs with blinks or horizontal eye movements were rejected
from analyses.
Fig. 1. Summary of measurements from average evoked potentials during the
balance and flanker tasks. A: balance: average data from FCz and a representative single trial of perturbation-evoked muscle activity (full wave rectified)
from gastrocnemius are displayed. Onset of perturbation is measure from cable
release force. N1 response latency is denoted from the onset of perturbation to
the timing of peak negativity. B: flanker: averaged data from FCz and
schematic of the stimulus onset and response timing used to denote reaction
measurements. Error-related negativity (ERN) response latency is denoted
from the onset of response to the timing of the peak negativity.
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Electroencephalography (balance and flanker tasks). To quantify
cortical activity, evoked potentials were recorded using a 64-channel
electrode cap (Neuroscan, El Paso, TX), based on the 10 –20 system
of electrode placement. All channels (EEG and electrooculography)
were prepared to maintain impedance ⬍5 k⍀. Signals were filtered
(DC-300 Hz) online using a SynAmps2 amplifier (Neuroscan) and
were sampled at a rate of 1,000 Hz.
The Polhemus Tracking System (3DSpaceDX; Neuroscan) was
used to digitize the precise position of the 64 electrode sites on each
participant’s head, creating a three-dimensional (3D) image. The
coordinates of the participant’s left and right preauricular notches and
nasion were used as the reference plane for all 64 electrode positions.
During postprocessing, these 3D coordinates (x, y, and z in mm) were
imported into CURRY 6 (Compumedics Neuroscan, Charlotte, NC)
and coregistered with the participant’s magnetic resonance image
(MRI) for source localization. Structural MRI was collected using
standard 3D high-resolution T1-weighted images that were acquired
during a separate session.
Balance reactions (electromyography, center of pressure, and
perturbation onset). To capture and characterize the onset of the
compensatory balance reaction, electromyography (EMG) was recorded from bilateral medial gastrocnemius (MG) and bilateral tibialis
anterior. EMG was also recorded from bilateral upper trapezius to
capture neck muscle activity to screen for possible artifact on EEG
tracings. Impedance was ⬍5 k⍀, measured at 30 Hz (Grass EZM5
Electrode Impedance Meter, Grass Instrument, Quincy, MA). The
signal was amplified ⫻1,000 with an isolated bioelectric amplifier
(AMT-8, Bortec Biomedical, Calgary, AB) and digitally sampled at a
rate of 1,000 Hz.
The center of pressure (COP) was recorded to characterize the
overall compensatory balance reaction by having the participants
stand on a force plate (Advanced Medical Technology, Watertown,
MA). In addition, cable force was recorded using a load cell to
measure the onset of perturbation and preperturbation lean force
(reflection of perturbation amplitude). The lean force was monitored
at the beginning of every trial to ensure that it remained consistent.
EMG, COP, and cable force were all digitally sampled at a rate of
1,000 Hz.
Reaction time and errors (flanker task). During the flanker task,
measures of the reaction times and errors were collected. Reaction
time was calculated as the time (ms) elapsed between the presentation
of the visual stimulus and the button press response. An erroneous
response was considered to have occurred if the participant indicated
by the appropriate button press that the target arrow was congruent
when it was incongruent or vice versa. Error rate (%) was calculated
by measuring the number of errors relative to the number of stimuli.
Data sampled for reaction time was collected at 1,000 Hz.
To characterize the N1 and ERN, the latency and amplitude of
postperturbation and posterror cortical potentials were measured for
each individual participant. Data were averaged across trials for each
individual with respect to the onset of the perturbation for lean and
release trials and the onset of the error for the flanker task. From each
individual’s averaged response, N1 and ERN latencies were determined by marking the time of the negative peak that occurred within
500 ms of the perturbation and error onset (time 0), respectively (see
Fig. 1). The amplitude of the N1 response was recorded as the
absolute amplitude at the negative peak while the amplitude of the
ERN was determined by calculating the difference in voltage between
that at the peak of the positivity preceding the negativity (i.e., onset of
the negativity) and that at the peak of the negativity. The mean
amplitudes and latencies of the N1 and ERN were calculated across all
participants. The number of trials averaged for the balance task (N1)
was typically between 35 and 40 trials with only a small number
excluded due to artifact. The number of the trials averaged for the
CORTICAL ACTIVITY AND BALANCE REACTIONS
standard deviation (SD) for a baseline preperturbation interval (first
1,000 ms of the trial) was established for each trial. The AP COP
onset was defined as the point at which it exceeded the confidence
interval (Mochizuki et al. 2008) and was reported as the time to AP
COP onset (ms) after the onset of the perturbation. The peak of the AP
COP excursion (within 500 ms of the AP COP onset) was detected,
and the amplitude of the AP COP response was then calculated as the
difference between the peak value and the mean baseline value.
RESULTS
Behavioral Data
Balance task. For the lean and release task, the mean
percentage of body weight for the cable force across was 5.5%
(SD 0.89). Compensatory balance reactions were present in all
trials, demonstrated by rapid MG activation and AP COP
excursions following the balance disturbances. The onset of
balance reactions averaged across 11 participants was 182.8 ms
(SD 14.8) and 183.7 ms (SD 12.6) for the left and right MG,
respectively. The average amplitude of the peak AP COP
excursion was 13.8 cm (SD 2.2), and the average time to peak
was 586.1 ms (SD 141.1) from the onset of perturbation.
Flanker task. Across the 11 participants, the average reaction times for the flanker task were 315.9 ms (SD 46.5) and
361.1 ms (SD 56.5) for correct responses to congruent and
incongruent stimuli, respectively. The average reaction time
for the incorrect responses to incongruent stimuli was 281.7 ms
(SD 42.4). Note that there were too few incorrect responses to
congruent stimuli to generate a meaningful average within all
participants. The average error rate across participants for the
congruent stimuli was 5.34% (SD 4.57) with three participants
having error rates ⬍1%. In contrast, the average error rate
across participants for responses to incongruent stimuli was
20.6% (SD 9.4).
Electroencephalography
Cortical activity for each task condition was grand averaged
(across trials for each participant and then across all 11 participants). A clear N1 and ERN were evoked in response to the
perturbations during the balance task and errors made during
the flanker task, respectively. The mean latency for the peak of
the N1 response (at FCz) was 103.0 ms (SD 12.72) with mean
amplitude of 30.25 ␮V (SD 9.05). The mean latency for the
peak of the ERN (at FCz) was 24.0 ms (SD 16.82) with mean
amplitude of 16.06 ␮V (SD 7.62) (Table 1). Figure 2, A and B,
shows the grand averaged ERP waveforms during the balance
task and flanker task, respectively. The onset of the perturbations and the time of the button presses are denoted as t ⫽ 0
ms. A clear ERN was evoked during the flanker task in
response to error trials only. As stated previously, too few
errors were made on congruent trials to compute an average
waveform. Figure 3 shows the average topographic representation for the evoked potentials revealing the fronto-central
representation of both the N1 (balance task) and ERN (flanker
task).
Source Localization
The comparison of source localization was possible among
9 of the original 11 participants. In two participants noise made
it difficult to obtain reliable source localization. The dipole
results for one participant are displayed in Fig. 4, A (N1) and
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flanker task (ERN) was dependent on the frequency of errors for each
participant. Only one participant (participant 3) had a small number of
errors (24) and due to a poor signal-to-noise ratio (SNR), the analysis
of the ERN dipole was excluded. Analysis of the amplitude and timing
of both negativities was limited to the electrode site where the
amplitude of the negativity was maximal, typically FCz.
Source localization. To further reduce noise, each participant’s
averaged N1 and ERN waveforms were filtered using independent
component analysis (ICA). The ICA time interval was set using the
electrode site where the amplitude of the peak negativity was maximal. The time interval began at the positive peak immediately before
the negative peak following the onset of the perturbation (balance
task) or the onset of the error (flanker task). The time interval ended
at the positive peak immediately following the negative peak. To
determine the number of valid components for the ICA, principle
component analysis (PCA) was utilized. PCA components that explained ⬍4.0% of the variance were excluded from analysis. The ICA
components were then calculated based on the subspace selected in
the PCA. Determining the valid ICA components was based on the
degree to which the component appeared as the N1 or ERN waveform
(i.e., peaks occurring in phase), the topographic distribution (i.e.,
negative in the fronto-central region of the brain), as well as how it
contributed to the overall mean global field power (MGFP); a collapsed average and measure of signal strength (i.e., SNR) of all EEG
channels. The resulting filtered EEG data were utilized for source
localization.
Localization of the N1 and ERN was conducted separately for each
task condition and for each participant. For all participants, the noise
estimation was performed in an interval that had an average noise
level of ⬍1 ␮V and a maximum SNR ⬎10 ␮V. The images were
coregistered to each participant’s structural MRI and the 3D coordinates (x, y, and z in mm) of the electrode positions on their scalp. One
dipole was located using the fixed coherent model since the location
and orientation of the dipole were assumed fixed over the time interval
selected. Thus, for all time points, common positions and orientations
were fitted. The dipole analysis was performed on a 20-ms time
interval surrounding the peak negativity of the MGFP for each task
condition. The locations of dipole estimates for each task within each
participant were reported in Talairach coordinates (x, y, and z in mm).
The absolute distance between the N1 and ERN dipoles was calculated for each participant. The locations of the N1 and ERN dipoles
were considered different if the distance between them was greater
than the average EEG source localization error of 10.5 ⫾ 5.4 mm,
determined by Cuffin et al. (2001), using a realistic head shape model
(BEM) and implanted depth electrodes.
Perturbation onset and lean force. The perturbation onset was
determined from cable force data that was first filtered with a fourth
order low pass Butterworth filter (75 Hz). The mean amplitude (V)
and 99% confidence band were determined for a 500-ms time window
that began 750 ms before the onset of the perturbation. The time at
which the cable force exceeded the confidence band denoted the onset
of the perturbation. Cable force was also used to determine lean force
(related to lean angle) before the perturbation. This mean value was
then converted and reported as a percentage of body weight.
Electromyography. EMG data was filtered using a second order
band pass Butterworth filter (20 –250 Hz), baseline corrected, and
full-wave rectified. The mean amplitude and 99% confidence band
were determined for a 300-ms time window before the onset of the
perturbation (⫺300 – 0 ms). The latency of the initial EMG burst
following the perturbation was defined as the point at which the EMG
amplitude exceeded this 99% confidence band for 25 ms or longer.
Because the perturbations were delivered in such a way so as to cause
forward instability, only the EMG latencies for the bilateral MG were
calculated and reported.
Center of pressure. The anterior-posterior (AP) COP data were first
filtered with a fourth order low pass Butterworth filter (15 Hz). To
determine the onset of the AP COP excursion, the mean (cm) and
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CORTICAL ACTIVITY AND BALANCE REACTIONS
Table 1. Latencies and amplitudes of the evoked potentials at the FCz electrode site for the balance task (N1) and error trials during
the flanker task (ERN)
Balance Task: N1
Flanker Task: ERN
Latency, ms
Amplitude, ␮V
Latency, ms
Amplitude, ␮V
1
2
3
4
5
6
7
8
9
10
11
Means
95
115
84
101
105
125
93
89
117
110
99
103.0 ⫾ 12.72
35.40
22.27
23.02
36.40
27.23
54.03
28.27
25.89
28.24
25.25
26.71
30.25 ⫾ 9.05
38
5
30
6
31
44
4
0
34
43
29
24.0 ⫾ 16.82
12.65
16.53
5.18
22.83
21.10
16.70
8.76
13.11
33.37
14.14
12.35
16.06 ⫾ 7.62
Values are means ⫾ SE. The onset of perturbation during the balance task and the button press during error trials in the flanker task occurred at t ⫽ 0 ms.
ERN, error-related negativity.
B (ERN). Table 2 reports the summary results of the N1 and
ERN dipole Talairach coordinates (x, y, and z in mm). Note that
in all but one participant, the location of the N1 was associated
with medial frontal gyrus [Brodmann area (BA) 6]. The Talairach
coordinates for participant 11 were located in the paracentral
lobule. The average Talairach coordinates for the N1 were
localized to BA6. The interindividual source generators for the
ERN were more variable with 6/9 revealing source generators
in the cingulate gyrus. The average Talairach coordinates for
the ERN were localized to the cingulate gyrus (BA 24). The
mean resultant distance between N1 and ERN dipoles across
participants was 25.46 mm (SD 8.88). This distance is greater
Fig. 2. Grand average event-related potentials at FCz for balance task (A) and
flanker task (B). Time 0 corresponds to the time of onset of the perturbation for
the balance task and the button press for the flanker task.
than the average source localization error of 10.5 mm (SD 5.4)
determined by Cuffin et al. (2001).
DISCUSSION
The overall objective of the present research was to provide
a more detailed understanding of the specific neurophysiologic
events occurring at the cortex following a balance disturbance.
More specifically, the focus of this study was to determine
whether the perturbation-evoked N1 response was associated
with activity within the ACC. We were able to evoke typical
behavioral and electrophysiological responses during the two
tasks (balance task and flanker task). However, in contrast to
the main hypothesis, the present results revealed that the dipole
location of the activation following the balance reaction (N1
response) corresponded to the medial frontal gyrus (BA 6),
rather than the originally hypothesized ACC. Importantly, this
study made direct comparisons within each participant to the
ERN, evoked during the flanker task, and associated source
location, which was determined to occur within the cingulate
Fig. 3. Average topographic representation for balance task (A) and flanker
task (B). The timing is with respect to the onset of perturbation for the balance
task and the onset of the error response for the flanker task. The peak N1
occurred on average at 103 ms after the perturbation and the peak ERN
occurred on average at 24 ms after the error response.
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ID No.
CORTICAL ACTIVITY AND BALANCE REACTIONS
Balance task
B
Flanker task
Fig. 4. Axial (left), coronal (middle), and sagittal (right) image results of the single fixed coherent dipole for the N1 and ERN for participant 10. A: balance task:
N1 dipole was located in the medial frontal gyrus with Talairach coordinates of (5.0, ⫺16.6, 53.6) mm. B: flanker task: ERN dipole was located in the cingulate
gyrus with Talairach coordinates of (9.1, 20.9, 28.2) mm.
cortex (BA 24). The latter is consistent with previous literature
(Badgaiyan and Posner 1998; Carter et al. 1998, 2001; Dehaene et al. 1994; Gehring 1992; Gemba et al. 1986; Holroyd
et al. 1998; Kerns et al. 2004; Kiehl et al. 2000; Menon et al.
2001; Miltner et al. 1997, 2003; Niki and Watanabe 1979;
Shima and Tanji 1998; Ullsperger and von Cramon 2003).
Electroencephalography
While this was the first study to localize the N1 response
during balance reactions, the polarity, latency, amplitude, and
topographic representation of the peak of the measured N1
response were comparable with those reported in the literature
(Dietz et al. 1984, 1985; Dimitrov et al. 1996; Duckrow et al.
1999; Mochizuki et al. 2010; Quant et al. 2004a, 2004b;
Staines et al. 2001). Note that similar to previous work, the N1
represents a very large amplitude signal (often ⬎50 ␮V),
which likely maximized the ability to localize the source dipole
due to an excellent SNR. The consistency of this potential
across such a range of different perturbation conditions, as
noted in the introduction, also speaks to the robust nature of
this potential.
While we did localize the ERN to the ACC as previous
reported, we did observe a difference in one property when
comparing the ERN evoked in this study during the flanker task
and other studies. While the polarity, amplitude, and topographic representation of the ERN were similar, the latency of
the ERN peak was shorter in the present study (21.1 ms SD
16.4 following the onset of the error) compared with what is
typically found in the literature (50 –150 ms following the
onset of the error) (Falkenstein et al. 1990; Gehring et al. 1990,
1993; Gemba et al. 1986; Miltner et al. 2003; Sasaki and
Gemba 1986). However, Fiehler et al. (2005) reported earlier
ERN latencies in a proportion of individuals who were not
instructed to correct their errors, but did so, nonetheless. It is
possible that the participants in the present study similarly
performed uninstructed corrections, thus contributing to an
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A
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CORTICAL ACTIVITY AND BALANCE REACTIONS
Table 2. Talairach coordinates and distance between N1 (balance task) and ERN (flanker task) dipoles
Dipole Talairach Coordinates (x, y, z), mm
ID No.
Balance task: N1
Flanker task: ERN
Distance Between Dipoles, mm
1
4
5
6
7
8
9
10
11
Means
(3.2, ⫺6.3, 56.8)
(11.7, ⫺10.0, 51.5)
(2.1, ⫺14.9, 57.1)
(⫺12.3, ⫺9.2, 63.4)
(⫺4.7, 11.9, 44.0)
(6.3, ⫺27.9, 44.9)
(⫺2.7, ⫺16.8, 64.0)
(5.0, ⫺16.6, 53.6)
(3.7, ⫺16.5, 48.3)
(5.74, ⫺11.8, 53.7)
(⫺12.9, 11.9, 42.6)
(⫺2.8, ⫺8.8, 59.0)
(5.2, ⫺12.4, 43.0)
(5.4, ⫺5.7, 46.9)
(⫺7.1, ⫺19.7, 37.4)
(⫺7.3, ⫺12.1, 31.2)
(⫺4.2, ⫺0.3, 56.0)
(9.1, 20.9, 28.2)
(⫺4.2, ⫺13.5, 26.2)
(6.47, ⫺4.41, 41.17)
28.1
16.4
14.6
24.5
32.4
24.9
18.4
45.5
23.7
25.46 ⫾ 8.88
Values are means ⫾ SE. Note that participants 2 and 3 were excluded from source localization due noise.
Behavioral Data
The behavioral results (i.e., EMG and COP) for the balance
task reveal that the lean and release protocol reliably evoked
feet-in-place compensatory balance reactions with characteristics comparable to those reported in literature (e.g., Adkin et al.
2006; Mochizuki et al. 2008, 2010). The EMG and COP onset
latencies were slower than some previous work, most likely
due to the smaller amplitude of perturbation used in this study.
The amplitude of perturbation is associated with the initial lean
angle, and in this study we set out to limit the compensatory
balance reactions to feet-in-place responses, requiring a relatively small initial lean angle. As a result, the amplitude of
perturbation was smaller than studies such as Mochizuki et al.
(2010) who focused on stepping reactions. However, our data
are in line with work of Adkin et al. (2006) who focused on
smaller amplitude perturbations.
For the flanker task, the reaction times were comparable to
those reported by Ullsperger and von Cramon (2001) for a
similar speeded modified flanker task. The mean reaction times
for the present study were 315.9 ms (SD 46.5) for congruent
correct trials, 361.1 ms (SD 56.5) for incongruent correct trials,
and 281.7 ms (SD 42.4) for incongruent incorrect trials. Similarly, Ullsperger and von Cramon (2001) reported mean reaction times of 323.0 ms (SD 6.8) for congruent correct trials,
378.0 ms (SD 6.1) for incongruent correct trials, and 283.0 ms
(SD 7.9) for incongruent incorrect trials. Higher error rates and
longer reaction times for incongruent trials indicate that participants had more difficulty during trials with a higher response conflict (Ullsperger and von Cramon 2001).
Interpreting the Dipole Location: ERN vs. the Perturbation
Evoked N1 Response
As noted above, the behavioral and electrophysiological data
confirm that we evoked responses comparable to previous
work. However, as highlighted earlier, the source localization
revealed a different underlying dipole (ACC for the ERN and
BA 6 for the N1). This difference has countered the original
hypothesis that the N1 would originate from the ACC. The
question becomes what is the potential interpretation of the N1
in light of a source localized to the medial frontal gyrus (BA 6).
BA 6 is comprised of two premotor cortical regions, the
premotor cortex laterally and the SMA medially. In addition,
while there was some interindividual variability potentially due
to measurement error or between subject variation in absolute
spatial locations, it is speculated that the generator of the N1
response is the SMA. This is based on the resulting mean
Talairach coordinates, (5.74, ⫺11.81, 53.73) mm, and Talairach label, medial frontal gyrus (BA 6), of the N1 dipole in
the present study.
In accordance with the known function of the SMA, it could
be thought that that the N1 response represents sensory processing of the balance perturbation (Dietz et al. 1984; Quant et
al. 2004b). However, as stated previously, Mochizuki et al.
(2008) demonstrated that the amplitude of the N1 response is
strongly influenced by temporal predictability of the perturbation, independent of the evoked sensory discharge linked to the
perturbation. When the perturbation magnitude was held constant (i.e., providing the same amount of sensory input across
perturbations), the ability to predict the onset timing of the
perturbation attenuated N1 amplitude, compared with temporally unpredictable perturbations (Mochizuki et al. 2008). It has
been speculated that an earlier evoked potential, the P1 response, which occurs ⬃40 –50 ms following the onset of the
perturbation, in fact represents the sensory information of the
perturbation since its maximum amplitude is topographically
located over the primary sensory cortex (Jacobs and Horak
2007). Integration of the perturbation related sensory information (e.g., visual, vestibular, and somatosensory) occurs over a
distributed network involving the temporal, parietal, and insular cortices (Blanke et al. 2000; Brandt et al. 1994; de Waele et
al. 2001; Jacobs and Horak 2007; Perennou et al. 2000). Thus
it is likely that the N1 response does not simply represent the
sensory processing of the perturbation.
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earlier ERN latency. Although this is a plausible explanation
for the decrease in ERN latency, one must also consider that
there is generally far more variability across participants in the
timing of the ERN (as compared with the N1), which is likely
due to the fact that the alignment of the waveform to the motor
response (i.e., pressing the mouse button) is not a precise reflection of the “detection” of an error. The variability of the timing of
the ERN in the current study appears to overlap within ranges of
other studies even though the mean tendencies are different.
Regardless of the mean timing differences, the similarities in the
associated topographic representation and the source localization
suggest that the underlying source of the ERN in this study was
similar to previous work.
CORTICAL ACTIVITY AND BALANCE REACTIONS
but the amplitude of it scales to the temporal predictability
(Adkin et al. 2006; Mochizuki et al. 2008) and consequence
(Mochizuki et al. 2010), such as the size (e.g., Mochizuki et al.
2010; Staines et al. 2001), of the perturbation. While Adkin et
al. (2006) demonstrated that the N1 is completely abolished
when the perturbation was temporally predictable, more recent
studies have demonstrated that the relative amplitude is, rather,
attenuated (Mochizuki et al. 2008, 2010). In a predictable
perturbation, preparatory cortical activity begins before the
onset of the perturbation (Jacobs et al. 2008; Maeda and
Fujiwara 2007, Mochizuki et al. 2008, 2010; Yoshida et al.
2008), as demonstrated by a negative slow-wave DC shift in
the EEG waveform beginning as early as ⬃1200 ms before the
onset of the perturbation (Mochizuki et al. 2008, 2010). Since
the preperturbation preparatory activity (Jacobs et al. 2008;
Mochizuki et al. 2008, 2010) and the N1 response (Dimitrov et
al. 1996; Duckrow et al. 1999; Quant et al. 2004b) are maximal
over the same electrode site, a relationship could exist between
their underlying cortical processes (Mochizuki et al. 2010). It
is speculated that the N1 amplitude is attenuated in predictable
perturbations because modifications to central set, to generate
optimal reactions, occurred before the perturbation based on
the perceived amount of threat.
Alternatively, the N1 responses localized in the region of the
SMA may also reflect more generic processing such as that
proposed by Ullsperger and von Cramon (2001). It has been
suggested that the ERN is linked to a reinforcement learning
process where the basal ganglia monitors behavior and the
ACC decides which competing mental process gains access to
the motor system (Holroyd and Coles 2002). When the behavior is worse than expected, the basal ganglia signals the ACC
of the error by decreasing its dopaminergic innervation, transiently preventing its inhibitory influence on the ACC, resulting in the ERN (Holroyd and Coles 2002). Another theory
related to competing processes suggests that the ERN represents a response conflict monitor (Carter et al. 1998; Miltner et
al. 1997; van Veen and Carter 2002a,b; Yeung et al. 2004). As
a response conflict monitor, the ACC detects, during error
trials, that incompatible processes are active at the same time
(i.e., conflicting activation of the rapid erroneous response and
slightly slower correct response, which emerges due to ongoing evaluation of the stimulus) (van Veen and Carter 2002a,b).
However, Ullsperger and von Cramon (2001) demonstrated
that monitoring response conflict and detecting errors are two
different systems since cortical activation during error trials
was different than the activation during correct trials with high
response conflict. Pre-SMA was activated during correct trials
with high response conflict, suggesting that it has a role in
overcoming obstacles between the planning and execution of a
motor action before the action actually occurs (Ullsperger and
von Cramon 2001), whereas, during error trials, the ACC was
activated, suggesting that it has a role in detecting an error once
it has occurred and potentially uses the information to correct
the error (Ullsperger and von Cramon 2001).
Another explanation could be attributed to previous reports
indicating that the source of the ERN and error-related responses appear to be task dependent. As examples, Reinhart et
al. (2012) noted differences in the contributions of the ACC
and SMA for manual vs. saccade tasks, while Mars et al.
(2005) suggested that the activation of the ACC vs. (pre-) SMA
could be related to external error feedback processing vs.
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It is possible that the N1 response is linked to the execution
of the motor response to counteract the loss of stability with a
SMA generator because the premotor regions are expected to
play a role in the execution of movements due to their direct
projections to the spinal cord via the corticospinal tract. However, based on the results of the ankle pendulum study by
Quant et al. (2004b) it was concluded that the N1 is not simply
linked to the execution of motor responses. Quant et al.
(2004b) compared N1 responses when participants were asked
to either react or not react to the perturbation (active vs.
passive) and discovered that large amplitude N1 responses
were apparent even when compensatory balance reactions were
absent. This leads to the view that the N1 is not explicitly
linked to the execution of motor responses since there was no
muscle activity. In addition, Mochizuki et al. (2010) also
suggested that the N1 is not associated with the execution of
the initial balance reaction, specifically that the timing of the
peak N1 response remains relatively consistent across different
perturbation amplitudes, directions, and initial positions of the
individual, despite the fact that the onset latencies of the
compensatory muscle activity and COP excursions vary substantially.
The fact that the peak N1 response does not always precede
the onset of the motor response supports the idea that there are
different phases of the compensatory balance response. The
initial, short-latency phase of the compensatory balance response is automatic (Jacobs and Horak 2007; McIlroy et al.
1999) and composed of automatic spinal reflexes that briefly
activate distal leg muscles (Ackermann et al. 1991). However,
since these reflexes are inadequate for regaining stability (Jacobs and Horak 2007), peripheral sensory information evoked
by the balance disturbance consecutively elicits preset synergies stored within the brainstem to activate stabilizing muscles
throughout the body. There is evidence to support the claim
that the earliest phases of the balance response may not include
transcortical loops (e.g., Ackermann et al. 1991; Berger et al.
1990; Dietz et al. 1984, 1985; Honeycutt et al. 2009; Quintern
et al. 1985). Similarly, only the later phases of the compensatory balance response appear to require attentional resources
(i.e., involvement of the cortex), as attentional shifts away from
a dual task only occurred 200 –300 ms following the onset of
a balance reaction that began ⬃90 ms following the onset of
the perturbation (McIlroy et al. 1999). It is possible that later
phases of compensatory balance responses involve the cerebral
cortex and that they are then modified to fit the characteristics
of the perturbation, the environmental surround, and the intentions of the individual (Beloozerova et al. 2003, 2005; Burleigh
and Horak 1996; Chan et al. 1979; Norrie et al. 2002; Taube et
al. 2006). Thus the N1 may represent the involvement of the
SMA, along with the prefrontal cortex, in generating a motor
plan to shape the later phases of the compensatory balance.
Literature has shown that the elements of compensatory balance reactions involve the primary motor cortex (Beloozerova
et al. 2003; Bolton et al. 2011, 2012; Jacobs and Horak 2007;
Taube et al. 2006), which may indirectly support a potential
sensorimotor role for a SMA generated N1 response.
Further evidence supporting the suggestion that the N1
represents the planning of the later stages of the compensatory
response based on what is required to regain stability may
come from the fact that the timing of the N1 response remains
consistent (Mochizuki et al. 2009a, 2010; Quant et al. 2004b)
2641
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CORTICAL ACTIVITY AND BALANCE REACTIONS
internal error detection. Potential differences in the roles of the
ACC and SMA have also been associated task difficulty
(Gallea et al. 2008). The results of the present study may
similarly reflect task-dependent dissociations between the
SMA and ACC for balance-related and nonbalance-related
tasks, respectively. Similarly, it is possible that a distributed
network underlying error-related negativity may be characterized by task-specific activation of these different cortical regions. This in turn could contribute to a measured shift in the
source location of the time-locked potential as measured in the
current study and simply represent a task-specific variation in
the expression of ERN processing.
Conclusion
GRANTS
This study was supported by the Natural Science and Engineering Research
Council of Canada.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: A.M., G.M., and W.E.M. conception and design of
research; A.M. performed experiments; A.M. analyzed data; A.M., G.M.,
W.R.S., and W.E.M. interpreted results of experiments; A.M. prepared figures;
A.M. and W.E.M. drafted manuscript; A.M., G.M., W.R.S., and W.E.M. edited
and revised manuscript; A.M., G.M., W.R.S., and W.E.M. approved final
version of manuscript.
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