Journal of Behavioral and Brain Science, 2011, 1, 160-166
doi:10.4236/jbbs.2011.13021 Published Online August 2011 (
Copyright © 2011 SciRes. JBBS
Inhibition in ActionInhibitory Components in the
Behavioral Activation System
Stefan Sütterlin1, Stein Andersson2, Claus Vögele1
1Integrative Research Unit on Social and Individual Development (INSIDE),
University of Luxembourg, Luxembourg City, Luxembourg
2Oslo University HospitalRikshospitalet, Oslo, Norway
Received June 8, 2011; revised July 19, 2011; accepted July 26, 2011
Over the past two decades, the neurobiological substrates of the reinforcement theory have been discussed in
terms of a behavioral activation system (BAS) and a behavioral inhibition system (BIS). While the BAS has
been conceptualized as both an activating system and an approach-related system, the empirical evidence for
either approach remains inconclusive. In the current study we hypothesize that the inclusion of self-regula-
tory capacity contributes to a better understanding of the BAS. In a sample of 29 volunteers motor response
inhibition elicited by a stop-signal task and heart rate variability (HRV) as a proxy of self-regulatory capacity
were related to BAS scores (BIS/BAS scales [1]). Results show significant positive associations between
inhibitory capacity and the sensitivity of the behavioral activation system, suggesting markers of self-regu-
lation as components of the BAS.
Keywords: Behavioral Activation System, Heart Rate Variability, Stop-Signal Task, Self-Regulation
1. Introduction
Over the past two decades, extensive research has been
conducted to investigate the reinforcement sensitivity the-
ory [2,3], its neurobiological substrates, related personality
traits [4] and psychopathology [5], and physiological in-
dicators. In the original formulation of their model, Gray
and colleagues [2,3] suggested a behavioral activation
system (BAS) and a behavioral inhibition system (BIS),
which are typically operationalized with the BIS/BAS-
Scales [1] at self-report level. However, based on their
research on the neurobiological substrates of these sys-
tems, Sutton and Davidson [6] conceptualized the be-
havioral approach system (BAS), which is opposed to
the behavioral inhibition system (BIS). If the BAS scales
indeed measure behavioral activation, independent from
behavioral direction, and in the more comprehensive sense
of intended alterations of spatial proximity (approach or
active avoidance), then this would be contrary to purely
approaching behavior. BAS scores should, therefore, be
positively related to physiological indicators of efficient
self-and emotion-regulation. Self- regulation describes
the individual’s ability to adapt behaviorally, emotionally
and cognitively to constantly changing environmental
demands. This includes goal-directed behavior, the abil-
ity to resist temptations, to overcome competing or pre-
potent action tendencies, to make elaborated decisions in
order to regulate emotional, cognitive and motor res-
ponses to optimize future outcome (overview [7]). Self-
regulation is conceived as a personality trait and can be
objectively assessed under laboratory conditions, typi-
cally via physiological and behavioral indicators of pre-
frontally mediated inhibitory control mechanisms, using
motor response paradigms. Motor response inhibition
paradigms, such as the stop-signal task (SST), induce
suppression of automatized, pre-potent motor behavior in
pre-defined, infrequent and unpredictable cases; they
require focused attention, stimulus discrimination, choice
of the appropriate reaction and its execution. These pro-
cesses can be subsumed under the broader term execu-
tive functions. In the present study it is hypothesized that
performance in a motor response inhibition paradigm is
positively associated with BAS scores.
Resting vagal tone has been identified as a peripheral
physiological correlate of BAS scores. Early research
reported a positive relationship between approach-related
Copyright © 2011 SciRes. JBBS
behavior and resting vagal tone [8,9], preparing the
ground for later findings with Carver and White’s [1]
BAS-scale by researchers comparing physiological meas-
ures and BAS scores [10,11]. The positive relationship
between vagal tone and BAS scores has been interpreted
in terms of mechanisms of emotional, self-regulatory,
and behavioral processes, according to the evolutionary
theory proposed by Porges [12-14]. Nevertheless, vagal
tone at rest can also be conceived as a measure of self-
regulatory and inhibitory capacity. Executive functions
and their association with regulatory competence and
their corresponding neurophysiological substrates have
been outlined in a model of neurovisceral integration,
which is complementary to Porges’ more philogenetic
approach. The model of neurovisceral integration de-
scribes inhibitory cortico-cardiac interactions mediated by
the vagus nerve and supported by the inhibitory trans-
mitter γ-aminobutyric acid (GABA) [15-17]. A first aim
of the present study was to replicate the reported positive
association between vagal tone and BAS scores. The
main aim of the present study, however, was the investi-
gation of the role of inhibition in the organization of cog-
nition, behavior and affect. Inhibitory processes are a
crucial component of behavioral adaptation. In the pre-
sent study measures of inhibitory capacity are operation-
alized as motor response inhibition performance (per-
centage of correctly inhibited motor responses), inhibi-
tory speed (stop-signal reaction time), and heart rate va-
riability (HRV), the latter indicating vagally mediated in-
hibitory cardiac control. We hypothesize that these mea-
sures of inhibitory control show a positive association
with BAS scores, thus supporting the assumption of BAS
resembling a behavioral activation system, which is
closely linked to executive functions tapping inhibitory re-
sources required for action planning and control.
2. Materials and Methods
2.1. Participants
Twenty-nine healthy participants (20 women, 9 men)
were recruited via advertisement from the staff of the
Oslo University Hospital. Age ranged from 19 to 47
years (M = 29.3, SD = 6.5). Participants received a fi-
nancial compensation for taking part in the study. Exclu-
sion criteria were self-reports of current and previous
psychiatric, neurological, or cardiovascular diagnoses,
and medication affecting the central nervous or cardio-
vascular system. The study was approved by the Re-
gional Ethical Committee of South-Eastern Norway and
all subjects gave written informed consent to participate,
in accordance with the Helsinki Declaration of 1975 (as
revised in 1983).
2.2. Material and Experimental Tasks
Stop-signal task: The “GO” stimuli consisted of the let-
ters “S” or “B”, presented on a 19-inch computer display
using E-Prime software (v2.0, Psychology Software
Tools, Pittsburgh, PA, 2007). Stimuli were presented in
black on white background, viewing distance from the
screen was 80 - 90 cm. Stimuli covered an angle of ap-
proximately 3.5˚ × 2˚ of the visual field. “GO” stimuli
were presented for 500 ms, followed by an intertrial in-
terval (ITI) of 1500 ms. The total number of trials was
600; in 150 trials (25%) the “GO” stimulus was followed
by an acoustic signal (1000 Hz, 500 ms) acting as a stop
signal. Stimulus onset asynchrony (SOA) between “GO”
and “STOP” signal was 100 ms, 200 ms, or 300 ms, as
determined by a performance-related staircase-tracking
algorithm [18], ensuring a similar level of subjective
difficulty of about 50% accuracy for all participants. Par-
ticipants were instructed to press a button as fast as pos-
sible as soon as either letter appears on the screen, but to
inhibit their response in those cases where the auditory
stop signal occurred. Recovery breaks after 200 and 400
items provided the possibility to relax.
2.3. Physiological Assessment
Electrocardiographic recording: Electrocardiogram (ECG)
was monitored using the Einthoven configuration with
disposable electrodes attached to the non-dominant wrist
and the opposite ankle. To reduce the probability of move-
ment artifacts and ensure regular breathing cycles par-
ticipants were instructed to relax and close their eyes
while monitoring ensued for a period of 10 min. ECG
raw data were recorded using a Neuroscan polygraph
(Neuroscan, Charlotte/NC), sampled at 512 Hz.
2.4. Data Reduction and Statistical Analysis
Stop-signal task: Stop-signal reaction time (SSRT) and
percentage of correctly suppressed reactions in “STOP”
trials were calculated following the recommendations
made by Logan (for details see: [19,20]), collapsing the
rank-ordered reaction times of “GO” trials into a single
distribution where the SSRT is identified on basis of the
probability of a response in “STOP” trials. This process
is repeated for each stop signal delay for each subject.
The results are then averaged over subjects within and
sometimes cross stop signal delays. Stop-signal reaction
time estimates the speed of the inhibitory process in mil-
liseconds, with lower value reflecting faster inhibitory
Vagal tone: offline analyses of ECG included the ex-
Copyright © 2011 SciRes. JBBS
traction of QRS complexes and subsequent identification
of interbeat intervals (IBI) from ECG recordings. Arti-
facts were identified according to the recommendations
from Berntson and colleagues [21] and real values esti-
mated via interpolation of neighboring IBI using ARTi-
iFACT software [22]. The last 5 min of the 10 min re-
cording session was chosen for HRV analysis in order to
ensure that data reflected resting conditions. Statistical
parameters of HRV [23,24] were calculated using AR-
TiiFACT. Time domain measures included mean heart
rate, RMSSD (square root of the mean squared differ-
ences of successive NN intervals) and pNN50 (the pro-
portion derived by dividing NN50 by the total number of
NN intervals (NN intervals: elapsed time between sub-
sequent ECG-R-peaks in milliseconds). Spectral fre-
quency measures were derived using Fast Fourier Trans-
formation (FFT). Frequency bands were labeled as rec-
ommended by the Task Force [24] as high frequency (HF,
0.15 - 0.4 Hz) and low frequency (LF, 0.04 - 0.15 Hz)
and expressed in power (ms2) and normalized units (n.u.).
Spectral frequency measures and time domain measures
were used as indicators for vagal tone and thus as phy-
siological markers of inhibitory capacity. LF/HF was
interpreted as a measure for autonomic balance, whereby
lower values indicate higher autonomic flexibility. All
measures of vagal activity were tested for normality.
Statistical analysis: BAS subscale and total scores [1]
were correlated with measures of vagal tone and motor
response inhibition. Intercorrelations between measures
of inhibition were calculated and tests for normality car-
ried out to ensure that criteria for multivariate analysis
applied. Where assumptions of normality were violated,
non-parametric correlations were conducted. Stop-signal
reaction time was tested for additionally explained vari-
ance in a stepwise multiple regression model with vagal
tone entered as first predictor, SSRT as second predictor.
The Statistical Package for Social Sciences (SPSS 17.0,
Chicago/IL) was used for all statistical analyses.
3. Results
Means and standard deviations for physiological and
behavioral measures of inhibition are summarized in
Table 1. The HRV and SSRT measures were all in a
range as previously reported in the literature [20,24-25],
as was the case for BAS scales “Drive” (M = 10.04; SD
= 2.15), “Fun Seeking” (M = 10.43; SD = 3.35), “Reward
Responsiveness” (M = 13.50; SD = 4.26), BAS total
score (M = 33.21; SD = 9.87) and BIS total score (M =
17.89; SD = 4.25) [1]. The analyses of associations
between measures of vagal tone (RMSSD, pNN50, HF
n.u., LF/HF) and BAS subscales “Fun seeking”, “Reward
responsiveness” and BAS sum scores showed significant
positive associations where measures of the time domain
were included (Table 2). In contrast, no such associa-
tions were found between frequency domain measures
and BAS scores. Non-parametric rank-correlations be-
tween HF (ms2) and BAS scores resulted in a similar
non-significant result as for the other frequency domain
measures. Moderate to medium effect sizes were also
found for the correlation of behavioral performance
(percentage of correctly inhibited stop-trials) and BAS
In a stepwise regression analysis including RMSSD and
SSRT the total variance explained by the predictor
RMSSD alone was 12.1% (2
R= 0.09), F(1,28) = 3.71,
p = 0.07. Inclusion of SSRT resulted in a 2
R= 0.09,
F(2,27) = 3.10, p = 0.09. Stop-signal reaction time was a
better predictor for BAS scores (standardized β = –0.315)
than RMSSD in a model including both predictors (β =
0.273). The resulting overall model (Figure 1) with inclu-
sion of both predictors resulted in 21.5% of explained
variance (2
R= 0.15, F(2,27) = 3.55, p = 0.04).
4. Discussion
The present results are in line with previous findings on
the association of vagal tone and BAS scores [10,11].
Time domain measures of vagal tone (RMSSD, pNN50)
showed significant correlations; however, frequency
domain measures of vagal tone did not reach significance.
RMSSD and pNN50 have been reported to be reliable
estimates of vagal activity at rest [23,24]. Nevertheless,
the present results replicate these previous findings only
partially and with reservations. The nature of the as
Figure 1. Scatterplot of regression model. Note: predicted
and observed BAS scores in the regression model with vagal
tone (RMSSD) and motor response inhibitory performance
(SSRT) as predictors (curved lines represent confidence
intervals to the mean).
Copyright © 2011 SciRes. JBBS
Table 1. Inhibitory measures.
n Min Max Mean SD
RMSSD 29 19.90 79.00 39.32 15.65
pNN50 29 1.00 54.20 20.76 17.12
HF (ms2) 29 58 555 217 150
HF (n.u.) 29 17.00 65.70 44.26 14.97
LF/HF 29 0.52 3.88 1.31 0.87
SSRT (ms) 29 134 279 201 38.35
Correct inh. (%) 29 25.79 94.83 55.77 18.54
Table 2. Correlations of inhibitory measures and BIS/BAS scores.
RMSSD 0.13 0.38* 0.35* 0.36* –0.10
pNN50 0.13 0.39* 0.34* 0.37* –0.03
HF (ms2) 0.02 0.10 –0.04 0.06 –0.08
HF (n.u.) 0.13 0.02 –0.16 –0.07 –0.20
LF/HF –0.09 –0.02 0.17 0.06 0.17
SSRT (ms) –0.20 –0.25 –0.37* –0.39* –0.23
Correct inh. (%) 0.41* 0.41* 0.38* 0.27 0.11
Note: values represent Pearson’s correlation coefficient r for all variables with the exception of HF
(ms2). Correlations with HF (ms2) are rank correlated (Spearman’s rs); * p < 0.05. ** p < 0.01,
(one-tailed). FS = fun seeking, RR = reward responsiveness.
sumed and previously reported association between
parasympathetic activation at rest and a pronounced be-
havioral approach or activation trait has not been specified
yet, with explanations limited to, e.g., “emotional, self-
regulatory, and behavioral processes” [11]. Vagal tone
reflects the activity of the X. cranial nerve, mediating the
cortico-cardiac modulation indicated by HRV. Neuro-
biological models have approached the phenomenon of
respiration-induced heart-rate oscillations at rest from
different perspectives. Previously, the philogenetic per-
spective suggested by Porges [12,13,26] was referred to
as an explanatory model for the observed association. In
the present study a different but complementary theo-
retical approach was taken by deriving explicitly inhibi-
tion-oriented hypotheses from the model of neurovisceral
integration [17] as a key process in the proposed central
autonomic network (CAN). This network has been de-
scribed as crucially depending on frontal inhibitory input
and includes GABAergic neuronal networks involved in
inhibitory action in emotional, cognitive, and behavioral
domains [15,17,27,28]. The CAN depicts a model of
neurovisceral integration, in which frontal inhibitory in-
put provides the means for self-regulated action and
regulated emotional responding via an extensive cortico-
cardiac network enabling the organism to adapt flexibly
to changing environmental needs, to focus attention, and
to facilitate executive functioning in terms of planning
and executing goal-directed behavior. Vagal activity is
known to be related to inhibition-intensive processing
such as working memory [29], and executive function
[17] and has recently also been shown to play a role in
higher-order decision-making processes such as over-
coming distracting emotional biases in individual or so-
cial context [30,31]. Based on the present results it is
argued that the association of vagal tone and BAS scores
is linked to frontal inhibitory capacity as a component of
Copyright © 2011 SciRes. JBBS
executive control. This interpretation is supported by the
positive relation on a behavioral level between stop-signal
reaction time representing effectiveness of inhibitory pro-
cesses interrupting pre-potent motor responses and BAS
scores. In the light of the present findings, previous no-
tions suggesting that vagal activity and the BAS scores
are positively correlated could be revised and extended
insofar as measures of inhibitory capacity are positively
related to BAS scores. We concede that further research
is needed to replicate these findings in larger samples,
possibly applying alternative measures of inhibitory ca-
pacity such as, e.g., antisaccadic eye-movements and be-
havioral measures of executive control.
The role of inhibitory processes for executive func-
tions might explain the close association with BAS scores.
Executive functions and their underlying components
such as goal-directed behavior, working memory, and re-
gulated emotional responding make intensive use of pre-
frontally originating inhibitory processes [32]. In contrast
to behavioral inhibition as indexed by the BIS-scale, the
BAS occasionally requires conscious decision-making and
self-regulatory competences mirrored in delay of gratifica-
tion, sequential action plans and higher-order processing.
Components of action control such as these are linked to
prefrontal functions and inhibition in particular. They
increase the likelihood of successful action and thus in-
crease the probability of behavior as assessed by the
Regarding the debate of BAS as a behavioral activa-
tion or behavioral approach system, the present findings
support the idea of a behavioral activation system re-
gardless of locomotive or motivational direction, defined
as either approach or active avoidance. The concept of
executive functions describes the neuronal and physio-
logical basis for consciously planned and goal-directed
behavioral competence regardless of its direction, exactly
as does frontal inhibition as indexed by performance in
the stop-signal task, inhibitory event-related potentials
and vagal tone. Inhibitory measures constitute the organ-
ism’s adaptability regardless of direction, but dependent
on prefrontal neuronal activity. The present study aimed
to contribute to the understanding of the mechanisms
underlying the behavioral activation system with par-
ticular respect to the nature of its postulated association
with vagal tone.
Recent research on relative frontal activation largely
supports the concept of a behavioral activation system. In
contrast to Sutton and Davidson [6], Harmon-Jones and
Allen [33] reported bilateral activity to be associated
with increased BAS scores. These findings were repli-
cated by Wacker and colleagues [34], suggesting that the
BAS is a behavioral activation system facilitating goal-
directed behavior regardless of direction. Further con-
firmation for the notion of a behavioral activation system
(as opposed to a behavioral approach system) comes
from a study by Hewig and colleagues [35]. In summary,
these results are in line with the earlier suggestion by
Gray and McNaughton [3] that active avoidance is part
of the BAS. Hewig and colleagues [35,36] dissected the
components of motivation and affective state, and re-
ported motivational direction to be associated with fron-
tal asymmetry, but behavioral activation per se to be re-
lated to greater bilateral activity.
Given the controversially discussed issue regarding
the operationalization of BIS/BAS and anterior asymme-
try, we restricted our research to the investigation of un-
derlying processes promoting relatively higher BAS-
scores. Our results suggest inhibitory capacity as an endo-
phenotypic trait marker of a pronounced behavioral acti-
vation system. We further suggest that the associations
for various markers of inhibitory measures reported in
the literature [10] and the results presented in the present
study are in line with the assumption of a behavioral ac-
tivation system, indicating higher behavioral regulation
competence in individuals scoring high on the BAS
Correlations of inhibitory measures and BIS score
were not subject to the present study. The lack of corre-
lations between inhibitory measures and the “behavioral
inhibitory system” might appear counter-intuitive. BIS
does not involve action, but the interruption and avoid-
ance of action. High BIS scores have been reported to be
associated with high reactivity to negative and poten-
tially threatening cues and anxiety [37], the opposite of
“regulated emotional responding”, which has been asso-
ciated with prefrontal function and vagal tone [17,27].
High BIS scores reflect poor emotion regulation. In con-
trast, the inhibition of behavior intuitively suggests a
positive association between physiological correlates of
inhibitory capacity and BIS scores, which is supported
by empirical data linking dorsolateral prefrontal cortex
(DLPFC) activity with BIS scores [38]. Heart rate vari-
ability is not a specific measure and involves the large
multilevel model of CAN. As such it is exposed to vari-
ous influences of diverging directions as they are re-
flected in BIS items. The BIS scale as it is conceptual-
ized does not find an equivalent in the CAN or inhibition
measures as such, particularly not a linear relationship.
5. Conclusions
The present results are in line with previous findings
reporting a positive association of vagal tone and BAS
score. This association was exceeded by a positive rela-
tionship of BAS score and motor response inhibition
performance as well as the stop-signal reaction time, a
Copyright © 2011 SciRes. JBBS
measure of inhibitory efficacy [19]. Taken together, both
measures of self-regulation and via inhibitory control
complement each other in predicting BAS scores on the
BIS/BAS scale. Thus, the positive association of inhibi-
tory capacity and BAS scores provide arguments for the
notion that the BAS represents a behavioral activation
system, not a behavioral approach system. Inhibitory
control is both, a key element of behavioral activation
and executive functioning.
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