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|  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.  Copyright © 2011 SciRes.                                                                                 JBBS  154  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-   C. HERBERT  ET  AL.  Copyright © 2011 SciRes.                                                                                 JBBS  155 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.  Copyright © 2011 SciRes.                                                                                 JBBS  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.     C. HERBERT  ET  AL.  Copyright © 2011 SciRes.                                                                                 JBBS  157 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   C. HERBERT  ET  AL.  Copyright © 2011 SciRes.                                                                                 JBBS  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).   6. References  [1] P. J. Lang, M. M. Bradley and B. N. Cuthbert, “Moti- vated Attention: Affect, Activation, and Action,” In: P. J.  Lang, R. F. 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