Journal of Behavioral and Brain Science, 2011, 1, 153-159
doi:10.4236/jbbs.2011.13020 Published Online August 2011 (http://www.SciRP.org/journal/jbbs)
Copyright © 2011 SciRes. JBBS
Response Inhibition and Memory Retrieval of
Emotional Target Words: Evidence from an
Emotional Stop-Signal Task
Cornelia Herbert1, Stefan Sütterlin1,2
1Department of Psycholo gy , University of Würzburg, Würzburg, Germany
2Integrative Research Unit on Social and Individual Development (INSIDE),
University of Luxembourg, Luxembourg, Luxembourg
E-mail: cornelia.herbert@psychologie.uni-wuerzburg.de
Received April 9, 2011; revised May 4, 2011; accepted June 20, 201 1
Abstract
Previous research suggests that emotional stimuli capture attention and guide behavior often automatically.
The present study investigated the relationship between emotion-driven attention capture and motor response
inhibition to emotional words in the stop-signal task. By experimental variations of the onset of motor re-
sponse inhibition across the time-course of emotional word processing, we show that processing of emo-
tional information significantly interferes with motor response inhibition in an early time-window, previ-
ously related to automatic emotion-driven attention capture. Second, we found that stopping reduced mem-
ory recall for unpleasant words during a subsequent surprise free recall task supporting assumptions of a link
between mechanisms of motor response inhibition and memory functions. Together, our results provide be-
havioral evidence for dual competition models of emotion and cognition. This study provides an important
link between research focusing on different sub-processes of emotion processing (from perception to action
and from action to memory).
Keywords: Emotion, Response Inhibition, Memory, Motivated Attention
1. Introduction
Response inhibition is an imp ortant key featur e of human
behavioral control. Response inhibition includes both,
inhibition of anticipated behavioral responses as well as
stopping of already initiated behavioral responses to
task-relevant stimuli. Regarding emotional stimuli, a
wealth of studies suggest that emoti onal compared to ne u-
tral stimuli capture attention and guide behavior auto-
matically [1]. Emotional stimuli are associated with ap-
proach and avoidance, i.e., action tendencies that pro-
mote individual survival and well-being [1]. Responses
to emotional stimuli should thus be generally harder to
inhibit compared to neutral stimuli because of their sur-
vival relevance. So far, a number of studies support this
assumption. Behaviorally, findings converge on a gen-
eral trend towards reduced performance when confronted
with emotional relative to neutral stimuli in tasks that
require response inhibition such as the go-nogo task
[2-4].
The stop-signal task (SST) [5,6] represents a paradigm
in which an already initiated response to task-relevant
stimuli has to be inhibited as quickly as possible. The di-
fficulty of response inhibition varies as a function of the
temporal delay between the target stimulus and the stop-
signal signaling the subject to stop his/her response.
The outcome of this race between responding and
stopping has recently been demonstrated to be modulated
by the stimulus’ emotional significance [7]. Verbruggen
and De Houwer [7] used emotional and neutral picture
stimuli and the stop-signal task. Pictures were of highly
arousing, unpleasant and pleasant content or of low arous-
ing neutral content and presented 500 ms before the on-
set of the target stimuli, which consisted of symbolic
items (geometric shapes). Reaction times to targets in
trials requiring no inhibition (go-trials) were sig nificantly
longer for targets preceded by emotional compared to
neutral pictures. In addition, processing of emotional com-
pared to neutral pictures significantly increased stop-sig-
nal reaction times (SSRT) to the neutral symbolic target
C. HERBERT ET AL.
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stimuli.
Although these results strongly support a relationship
between emotional processing and response inhibition,
the mechanisms that drive this relationship are still un-
clear. The SST is a behaviorally simple task; neverthe-
less, performance in the SST can be influenced by many
sub-processes. Verbruggen and De Houwer [7] suggested
that processing of emotional stimuli influen ces inhibition
of already initiated behavioral responses to task-relevant,
but neutral stimuli via attentional mechanisms. Theoreti-
cally, the grabbing of attentional resources by emotional
stimuli should influence both responding and inhibition of
motor responses to task-relevan t stimuli, b ecau se it l e aves
less processing resources available for the execution of
processes and actions that one is engaged in while the
emotional stimulus is processed [1].
Concerning visual processing of emotional stimuli
electrophysiological studies examining the time-course
of emotional stimulus processing propose that attention
capture by emotional stimuli occurs within two consecu-
tive time windows: A first time window starting as early
as 200 ms after emotional stimulus-onset and a second,
later time-window associated with more elaborate and
controlled processing of emotional stimuli [8-11]. Earlier
modulation <200 ms post stimulus-onset attributable to
stimulus-driven attention by emotional content has also
occasionally been reported, even with more symbolic
stimuli such as emotional words [12].
Taking these findings into account one may hypothe-
size effects of emotion on response inhibition to occur in
time-windows much earlier than those examined by Ver-
bruggen and De Houwer [7], where the temporal delay
between the onset of a picture and the stop-signal was
greater than 500 ms. Second, these effects should not be
restricted to picture stimuli of emotional content, but prin-
cipally also occur when emotional content is conv eye d b y
language stimuli [8,9].
The present study aimed to provide direct evidence for
these assumptions. Contrary to previous research [7] in
this study emotional and neutral words were used as tar-
gets of response inhibition in the SST and response inhi-
bition to emotional and neutral words was investigated
within the first 150 ms - 250 ms post stimulus onset.
Based on the findings reported above, we expected longer
reaction times to emotional co mpared to neu tral wo rd s o n
trials where no stop-signal is presented (go- trials). In
line with this, we expected stop-signal reaction time
(SSRT) to be increased for emotional compared to neu-
tral words indicating harder response inhibition to emo-
tional than neutral targets. Above all, we expected this
emotional-neutral SSRT effect to vary as a function of
the stimulus onset asynchrony (SOA) of the stop-signal
SOA and to interact with the emotional valence of the
words if processes required for successful response inhi-
bition are influenced by the early attention grabbing
power of the emotional target words.
A second issue addressed in the present study relates
to recent findings on a postulated association between
mechanisms supporting successful motor response inhi-
bition and memory. The need to control behavior is not
limited to inhibition of overt behavioral reactions but on
many occasions affords inhibition of unwanted cognitions
including unpleasant memories from coming to mind
[13,14]. Neuroimaging studies on response inhibition de-
monstrate enhanced activation of the dorsal and ventral
prefrontal cortex [15,16], critical for executive control
and behavioral regulation. Recent research by Anderson
and colleagues [17] suggested that activation in prefron-
tal executive control systems mediates hippocampal ac-
tivity and memory of unpleasant stimuli that participants
were asked to suppress during stimulus exposure. One
influential hypothesis derived from these studies is that
the potential mechanisms underlying memory inhibition
are analogous to those controlling overt behavior in reac-
tion time tasks. If this assumption is co rrect, to be stopped
items (in the stop-signal trials) should be spontaneously
remembered less frequently than to be responded items
(in the go-trials), in particular when their meaning is as-
sociated with unpleasant valence.
Based on the above reported literature the aims of the
present study can be summarized as follows: a) to exam-
ine the extent to which the emotional valence of a target
stimulus influences responding and motor response inhi-
bition in the SST at short latencies, b) to explore whether
memory retrieval of emotional targets is affected by
processes related to motor response inhibition.
2. Methods
2.1. Participants
Thirty-one healthy adult students (13 males, 18 females,
M = 24.0 years, SD = 3.0), all right-handed native
speakers of German participated in the study. Partici-
pants received course credit and gave written informed
consent to participate in the study. Written informed
consent was given in accordance with the ethical prince-
ples of the Declaration of Helsinki. Only participants,
who reported to be in good health (i.e., no current or his-
tory of drug abuse, chronic physical conditions, neuro-
logical diseases, mental ill health) and with normal sense
of hearing and normal or corrected to normal vision were
recruited. Participants had normal state, M = 39.0, SD =
7.8, and trait anxiety scores, M = 35.9, SD = 8.7, on the
Spielberger State and Trait Anxiety Inventory (STAI)
[18] and reported more positive than negative mood (po-
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sitive affect: M = 28.6, SD = 6.62; negative affect: M =
14.29, SD = 6.49) on the PANAS, positive affect, nega-
tive affect scales [19].
2.2. Stimulus Material
Experimental stimuli were 50 pleasant, 50 unpleasant,
and 50 neutral nouns which comprised on average six
characters and according to the CELEX data base [20]
were frequently used in German. Nouns were taken from
a word database previously collected by our own re-
search group1 that provides for each word mean valence,
arousal, and concreteness ratings of an independent sam-
ple of adult native speakers with comparable backgrounds
and ages to the participants of the presen t study. Valence
and arousal ratings were obtained on the Self Assessment
Manikin (SAM) [21], a culture-free, non-verbal rating
procedure. Concreteness ratings were obtained on a nine-
point SAM-like scale. Mean valence, arousal and con-
creteness scores as well as word length and word fre-
quency counts of the words are listed in Table 1. Pleas-
ant and unpleasant nouns did not differ significantly in
emotional arousal, but were both significantly more arous-
ing than neutral nouns. Mean valence ratings differed as
expected (pleasant > neutral > unpleasant). There were no
significant differences for concreteness, word length, or
word frequency across the three emotional categories (all
p > 0.2).
Stop-signal task: The SST was presented on a 19-inch
computer display using Presentation software (Neurobe-
havioral Systems Inc.). Nouns were presented in black
letters (font = “Times”; size = 40) centred on a white
background, the viewing distance from the screen was
80 - 90 cm. Half of the nouns of each category were as-
signed to the go-trials, the other half to the stop-trials.
Assignment of words to trials (go and stop) was random-
ized and counterbalanced across participants. Go-trials
were repeated 4 times; stop-trials two times resulting in a
total of 450 trials (75% Go, 25% Stop). Nouns were pre-
sented for 500 ms in each of the trials and followed by an
interstimulus-interval in which a fixation cross was dis-
played for 1200 ms - 1500 ms in the middle of the screen.
In the stop-trials nouns were followed by an acoustic
stop-signal (1000 Hz, 500 ms, sound pressure level 80
dB) promptin g participants to stop their response. Stimu-
lus onset asynchrony between the acoustic stop-signal
and noun-onset was 150 ms, 200 ms and 250 ms, respec-
tively. Each of the three stop-signal SOAs occurred
equally often. Go- and stop-trials with different SOAs
were presented randomly such that repeated words were
Table 1. Stimulus material characteristics.
Unpleasant Pleasant Neutral
Valence 2.63 (0.13) 7.33 (0.12) 5.31 (0.07)
Arousal 5.07 (0.12) 5.03 (0.10) 2.32 (0.08)
Concreteness4.17 (0.25) 4.78 (0.22) 4.20 (0.32)
Word length 6.20 (0.26) 6.96 (0.35) 6.88 (0.22)
Word frequency97.34 (31.35)144.92 (24.01) 129.96 (19.79)
Note: Mean valence, arousal and concreteness scores range from 1 (ex-
tremely negative valence, extremely low arousal or concreteness) to 9 (ex-
tremely positive valence, extremely high arousal or concreteness). Word
frequency counts for written language are based on the standardized word-
database CELEX [20]. Word length represents number of letters. Standard
errors are in parentheses.
nev er consecutive to avoid stimulus repetition induced by
short-term response time adjustment effects time adjust-
ment effects [22]. Presentation sequence of words from
the three different word categories shared convergence in
probability (i.e., each word of a category had the same
probabilit y to be followed by a word of th e same or a dif-
ferent word category).
2.3. Procedure
Upon arrival at the laboratory participants were seated in
a comfortable chair, gave written informed consent, they
were questioned about their health and filled in the self-
report questionnaires on mood (PANAS) [19], and state
and trait anxiety (STAI) [18]. Participants were given
detailed instruction concerning the SST. They were told
to respond to the words as quickly as possible by press-
ing a response key with the ind ex fing er of the right hand.
They were also told that on some trials a tone will occur
signalizing the stop-trial and the requirement to stop the
response to the target stimuli. Participants were asked not
to wait for the tone and respond to the targets as quickly
as possible. After the completio n of the SST, particip ants
were instructed to recall as many of the presented words
as they could remember in a surprise free recall test and
were debriefed about the purpose of the present study.
2.4. Data Reduction and Statistical Analyses
Stop-signal task: Stop-signal reaction time (SSRT) and
percentage of correctly suppressed responses (stop-signal
trials) were recorded and analyzed separately for the
three SOAs and word categories. Stop-signal reaction
time was calculated according to the algorithm proposed
by Logan [5,6], where SSRT is derived from the distri-
bution of response times to the go-trials, the observed
probability of responding in the stop-signal trials and the
stop-signal delay. Reaction time data (go-trials) and per-
1The complete list of words used in this study (original and translation)
together with valence and arousal ratings is available from the authors
upon request.
C. HERBERT ET AL.
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156
centage of correctly responded go-trials were analyzed
with repeated measurements of variance (ANOVA) con-
taining the factor “Valence” (unpleasant, pleasant, and
neutral) as within subject factor. SSRT and number of
correctly inhibited stop-trials were analyzed with repeated
measurements of variance (ANOVA) containing the fac-
tors “Valence” (unpleasant, pleasant, and neutral) and
“SOA” (SOA150, SOA20 0, and SOA250) as w ithin sub-
ject factors.
Memory Data-Free recall task: Participants’ memory
performance was analyzed with an ANOVA design con-
taining the factors “Trials” (go and stop) and “Valence”
(unpleasant, pleasant, and neutral) as within subject fac-
tors. Only correctly remembered words on successfully
to be responded and to be stopped trials were entered
into the analysis. For all measures reported above, sig-
nificant main effects and interaction effects were tested
with post hoc paired sample t-tests. p-values were cor-
rected using the Bonferroni adjustment.
3. Results
Stop-signal task: Participants responded on average cor-
rectly in 96% of the go-trials, regardless of whether nouns
were of unpleasant, M = 96.64, SD = 11.21, pleasant, M
= 96.06, SD = 11.08, or neutral meaning, M = 96.54, SD
= 11.32. Reaction times to successfully re- sponded
go-trials differed significantly as a function of word va-
lence, “Valence”: F(2,60) = 4.18, p < 0.01. Re- action
times in go-trials were significantly long er for unp leasan t
and pleasant compared to neutral nouns (unpleasant: M =
421.0, SD = 66.5; pleasant: M = 418.5, SD = 62.6; neu-
tral: M = 414.3, SD = 61.5), but did not differ signifi-
cantly between unpleasant and pleasant nouns (unpleas-
ant – pleasant: t(30) = –1.069, p = 0.29).
Number of correctly inhibited stop-trials varied sig-
nificantly with the SOA of the stop-signal, F(2,60) =
48.15, p < 0.001. On average, participants responded
more often to stop-trials the longer the SOA of the stop-
signal, demonstrating the increased difficulty of motor
response inhibition the longer the SOA of the stop-signal
[5]. Rate of correctly inhibited stop-trials was 73% at
SOA150 and close to 50% at both SOA200 (59%) and
SOA250 (45%), confirming SSRT as a reliable measure
of response inhibition [23]. Insignificant interaction ef-
fects of the factors “Valence x SOA” showed that this
was true for emotional as well as neutral nouns, “Va-
lence x SOA”: F(4,120) = 0.75, p = 0.5.
Stop-signal reaction time varied with the stop-signal,
“SOA”: F(2,60) = 10.47, p < 0.001 and, in addition,
showed a significant interaction of the factors “SOA”
and “Valence”, F(4,120) = 2.5, p < 0.05. For SOA250,
SSRT differed significantly between emotional and neu-
tral nouns: SSRT was significantly enhanced for emo-
tional compared to neutral nouns (unpleasant-neutral:
t(30) = 3.14, p < 0.01; pleasant-neutral: t(30) = 2.24, p <
0.05). Results are summarized in Table 2 and displayed
in Figure 1.
Memory Data-Free recall task: Emotional nouns, un-
pleasant and pleasant, were significantly better remem-
bered than neutral nouns (see Figure 2), indicating en-
hanced memory performance for emotional compared to
neutral items on later retrieval, “Valence”: F(2,16) = 18.3,
p < 0.01. Significant interactions of the factors “Valence
x Trial” and post hoc tests of the interaction effect, how-
ever, demonstrated that unpleasant nouns were remem-
bered less frequently when the corresponding responses
to them were successfully inhibited, “Valence x Trial”:
F(2,60) = 4.07, p < 0.05; unpleasant: t(30) = 2.40, p <
0.01.
4. Discussion
This study investigated response inhibition to emotional
and neutral target words in the stop-signal task at three
discrete stop-signal delays (SOA150, SOA200, SOA250)
and examined memory for emotional and neutral target
words as a function of response inhibition. Based on the
literature on the effects of emotion on attention [8-10,
24], we expected reaction times to emotional compared
to neutral words to indicate attention capture by emo-
tional relative to neutral words. We further hypothesized
attention capture by emotional stimuli to interfere with
response inhibition across the different SOAs. Processing
of unpleasant and pleasant nouns produced significantly
longer reaction times on go-trials compared to neutral
nouns. Stop-signal reaction time, as an index of response
inhibition, varied significantly as a function of both the
emotional valence of the words and the stop-signal delay.
For neutral nouns SSRT decreased from SOA150 to
SOA250. This decrea se in SSRT is a comm only rep orted
pattern (for an over vie w see [ 5] ). But fo r em ot i onal nouns
Table 2. Stop-signal reaction times (SSRT) and reaction
times in go-trials.
Stop-signal task (SST)unpleasant pleasant neutral
Reaction times (go-trials)421.0 (66.5) 418.5 (62.6) 414.3 (61.5)
SSRT (stop-trials)
SOA150 213.6 (34.8) 203.8 (51.1) 207.1 (41.4)
SOA200 188.2 (31.2) 184.2 (34.8) 186.6 (33.2)
SOA250 192.9 (44.2) 185.0 (51.7) 169.7 (37.4)
Note. Stop-signal performance including reaction times in go-trials and
SOA dependent SSRT as a measure of successful stopping and response
inhibition; measures are listed separately for unpleasant, pleasant and neu-
tral words. St andard deviations are i n p arentheses.
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Figur e 1. M o dul a tio n of S S RT b y s tim ulus valence a nd SOA (mean and standard errors).
Figure 2. Memory performance for emotional and neutral
nouns.
the decrease in SSRT across SOAs did not appear. For
emotional nouns relative to neutral nouns SSRT was sig-
nificantly increased at SOA250.
Previously, it has been speculated [7] that processing
of emotional stimuli interferes with response inhibition
because emotional stimuli capture more attentional re-
sources compared to neutral stimuli and therefore less
processing resources are available for successful inhibit-
tion of motor responses to the target stimuli. The results
of the present study provide further evidence in favor of
this speculation and suggest that attention capture by
emotional stimuli interacts with response inhibition at
even earlier time points than those examined previously.
Viewed from a biological perspective, such early effects
of emotion on response inhibition as reported in the pre-
sent study support du al competition models of cog nition,
emotion and motivation [25] that propose closely inter-
related and dependent processes involved in emotion
perception and response inhibition. Neurally, these ef-
fects could be accomplished by fronto-limbic connec-
tions biasing signal transfer from sensory association cor-
tex to prefrontal cortex and vice versa [25].
Our observation of an inhibition-dependent memory
effect for emotionally unpleasant targets is also in line
with dual competition models. Consistent with several
laboratory studies on emotional memory [26], emotional
nouns were post-experimentally better remembered than
neutral words. However, when free recall performance
was analyzed as a function of response inhibition, to be
stopped items were remembered less frequently than to
be responded items when their meaning was of negative
content. Anderson and colleagues [13,17] recently dem-
onstrated inhibition-related effects on later memory re-
trieval for unpleasant stimuli th at participants were asked
to inhibit and suppress during stimulus exposure. Based
on neuroimaging findings [17], the authors proposed a
potential link between processe s associated with memory
inhibition and inhibition of (motor) responses to un-
pleasant targets. To our knowledge, the present study is
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158
the first to examine this hypothesis directly by using a
motor response inhibition task and both emotional (un-
pleasant and pleasant) and neutral stimuli as targets of
response inhibition. Regarding unpleasant words, our
findings support the assumption of a relationship between
memory and inhibitory processes related to motor re-
sponse inhibition [13,14,17]. Interestingly, stopping had
no influence on recall of pleasant items. This also extends
previous research, as this study, contrary to the past
memory inhibition studies cited above, made use of stim-
uli of unpleasant as well as pleasant and neutral valen ce.
Although the reasons for the not impaired memory re-
trieval of positive target stimuli requires future research,
the finding fits n icely with everyday life experience: that
attempts not to respond to pleasurable or rewarding cues
(e.g., palatable food when on diet, expensive clothes
when short of money, etc.) does not necessarily weaken
the representation of these cues in memory.
In summary, our results provided evidence that proc-
essing and response inhibition of emotional targets in-
teract. These interaction effects appear to arise even at
very short latencies of 250 ms after stimulus onset, i.e., in
a time-window, where according to the previous lit- era-
ture early attention capture by emotional stimuli is ex-
pected to be most pronounced. In addition, our results
support a relationship between emotion-modulated motor
response inhibition and emotional memory. Future stud-
ies may offer further insight into the interplay between
the mechanisms supporting and attenuating response and
memory inhibition in emotion-laden contexts. Applica-
tion of this experimental approach to clinical samples
(e.g., drug addiction, eating disorder, or attention deficit
hyperactivity disorder) might be especially interesting to
this end [27].
5. Acknowledgements
This research was supported by the German Research
Foundati on (DFG).
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