Personality and Individual Differences 70 (2014) 131–135

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Personality and Individual Differences

journal homepage: www.elsevier .com/locate /paid

Emotional processing and frontal asymmetry in impulsive aggressiveindividuals

http://dx.doi.org/10.1016/j.paid.2014.06.0250191-8869/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +1 (254) 710 2236.E-mail address: matthew_stanford@baylor.edu (M.S. Stanford).

Sarah L. Lake, Matthew S. Stanford ⇑, Jim H. PattonDepartment of Psychology & Neuroscience, Baylor University, One Bear Place #97334, Waco, TX 76798-7334, United States

a r t i c l e i n f o

Article history:Received 28 October 2013Received in revised form 10 June 2014Accepted 16 June 2014

Keywords:ImpulsivityAggressive behaviorAlpha asymmetryEmotional control

a b s t r a c t

Right frontal cortical activity, thought to reflect increased activity in withdrawal-related systems, hasbeen observed in angry and anxious samples. The current study attempted to examine this effect inimpulsive aggressive individuals (IAs) and nonaggressive controls. Impulsive aggression is a reactive vio-lent response characterized by loss of behavioral control and previous physiological studies have foundIAs have sensory and informational processing deficits. In Study 1, undergraduate volunteers (n = 10 IAs,n = 14 controls) completed a resting EEG and IAs showed more right frontal cortical activity than controlsat rest. In Study 2, we replicated this result with undergraduate males (n = 15 IAs, n = 15 controls) anddemonstrated that not only did IAs have more right frontal activity at rest than controls, controls wereable to switch between the behavioral inhibition system (BIS) and behavioral activation system (BAS)depending on exposure to affective stimuli, whereas IAs could not. Results indicated IAs likely have anoveractive BIS, and thus have difficulty recognizing emotional stimuli, suggesting a dysfunction in emo-tional arousal. Future directions are discussed.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Impulsive aggression involves unplanned, immediate, violentresponses to minimal provocation (Stanford, Greve, & Gerstle,1997) and is considered reactive and emotional, accompanied bypoor regulation of physiological arousal as well as loss of behav-ioral control (Barratt, 1991; Houston, Stanford, Villemarette-Pittman, Conklin, & Helfritz, 2003). Neuropsychological findingshave demonstrated that impulsive aggression is correlated withexecutive dysfunction (Chambers, 2010), including a lack ofimpulse control (Stanford et al., 1997) and deficits in verbal strate-gic processing (Villemarette-Pittman, Stanford, & Greve, 2002).Along with executive functioning problems, individuals withimpulse control disorders frequently have comorbid anxiety aswell (Black, Shaw, McCormick, Bayless, & Allen, 2012; Carli et al.,2013; Kashyap et al., 2012). Additionally, impulsive aggressorshave a tendency to see most situations as threatening (Helfritz,2006), thus likely experience anxiety in both reinforcing and non-reinforcing situations.

One of the most difficult tasks humans often face is makingmotivational choices in response to reinforcing or nonreinforcingsituations. Stimuli in emotionally charged situations are oftenambiguous, and even if not, choices among behavioral alternatives

in response to those stimuli are uncertain in their outcomes—especially for impulsive aggressors. Gray (1978), Gray (1982),Gray (1990), Gray and McNaughton (2000) proposed threeseparate biological motivational control systems to underliehuman behavioral tendencies. Within the Reinforcement Sensitiv-ity Theory (RST), the degree to which a person finds specific stimulireinforcing drives their individual propensity to use each system:the Behavioral Inhibition System (BIS; the tendency to approachnegative stimuli), the Behavioral Approach System (BAS; thetendency to approach positive stimuli), or the Fight Flight FreezeSystem (FFFS; the tendency to avoid negative stimuli) (Gray &McNaughton, 2000). Both the FFFS and BIS are involved in defen-sive responses, but the FFFS is activated more selectively whenthreat is to be avoided, whereas the BIS activates whenever apotentially threatening situation is encountered (McNaughton &Corr, 2000; McNaughton & Corr, 2004; Perkins, Kemp, & Corr,2007). More simply, McNaughton and Corr (2004) use the termsdefensive avoidance when the FFFS is engaged and defensiveapproach when the BIS is activated.

The current study attempted to assess Gray’s RST using thephysiological measurement of frontal resting electroencephalo-gram (EEG) activity in an attempt to shed light on the motivationalunderpinnings of impulsive aggressors. Frontal resting EEG activityis mainly used to study individual differences related to trait ortrait-like measures in order to make inferences about emotionalprocesses (Davidson 1993; Davidson, 1998a; Davidson, 1998b;

132 S.L. Lake et al. / Personality and Individual Differences 70 (2014) 131–135

Davidson, Schwartz, Saron, Bennet, & Goleman, 1979). Davidsonand colleagues proposed that a difference in frontal symmetry atrest is indicative of a predisposition to approach a stimulus (andengage the BAS) if there is increased left frontal activity, or ten-dency to withdraw from a stimulus (and engage the BIS) if thereis increased right frontal activity. No studies have attempted tomeasure frontal resting EEG activity in impulsive aggressors,although Jaworska et al. (2012a) found that adults with dysfunc-tional anger showed increased right frontocortical activity at rest.Because anger and aggression are closely related (Buss & Perry,1992; Jensen-Campbell, Knack, Waldrip, & Campbell, 2007) andimpulsive aggressors generally have more anxiety than controls,in the current study we hypothesized that impulsive aggressorsshould have psychological measurements similar to individualswith anxiety disorders or dysfunctional anger (Fowles, 1988;Gray, 1982; Jaworska et al., 2012a; Ross, Keiser, Strong, & Webb,2013) and thus have increased right activity.

2. Study 1

2.1. Methods

2.1.1. Subjects and criteriaRecruited via posted print advertisements on a large private

university campus, participants first completed an online presc-reening evaluation that solicited information about participants’age, handedness, and medical history including previous majorhead injuries and current use of psychoactive medications. A totalof n = 365 participants aged 17–34 (M = 20.24, SD = 3.36) com-pleted the prescreening battery of self-report measures andn = 24 participants were invited to participate in the psychophysi-ological measurement portion of the experiment (describedbelow). Exclusion criteria included head injuries or history of anAxis I disorder. Additionally, because handedness has been hypoth-esized to affect asymmetry (e.g., Propper, Pierce, Geisler,Christman, & Bellorado, 2012), only right hand-dominant partici-pants were used. The Institutional Review Board at Baylor Univer-sity reviewed and approved the experimental protocol.

2.1.2. Participant selectionTo determine eligibility for participation in psychophysiological

measures, individuals completed an online prescreen survey. TheImpulsive Aggression Quick Screen (IA-QS; Stanford, Greve, &Dickens, 1995) is a short semi-structured interview that combines

Table 1Group differences in self-report measures in Study 1.

Controls IAs aMeasure M (SD) M (SD)

BPAQPhysical 14.36 (4.83) 32.50 (6.24)Verbal 10.86 (3.06) 19.10 (4.23)Anger 10.36 (3.30) 23.40 (4.40)Hostility 14.36 (5.40) 26.00 (8.00)Total 49.93 (13.83) 101.00 (14.94)

LHAAggression 3.57 (2.24)Self-Directed 0.29 (0.83) 14.50 (3.34)Consequences 0.36 (0.63) 2.40 (1.90)Total 4.21 (2.72) 3.80 (1.93)

20.90 (4.65)

BIS/BASBIS 13.10 (3.48) 15.00 (2.86)BAS Reward 7.60 (2.22) 8.50 (2.57)BAS Drive 8.50 (1.43) 9.21 (1.89)BAS Fun-Seeking 6.10 (1.66) 8.64 (1.91)

Note. Buss-Perry Aggression Questionnaire (BPAQ; Buss & Perry, 1992), Life History of AggScale (BIS/BAS; Carver & White, 1994). Negative t statistics indicate IAs reported higher

DSM-IV-TR criteria for Intermittent Explosive Disorder and self-identification of discrete episodes of aggression to determine cate-gorization into groups. To be classified as an Impulsive Aggressor(IA), individuals must have: (1) Identified several episodes ofbehavioral impulsive aggression with loss of behavioral controlin the previous six months; (2) The reported aggressive act(s)was disproportionate to the provocation; (3) At least 2 impulsiveaggressive acts occurred during the previous 30 days; and (4) Ascore of 8 or higher on the Irritability subscale of the Buss-DurkeeHostility Inventory (Buss & Durkee, 1957). This measure assessesan individual’s overall impression of his/her aggressive behaviorin the preceding six months and resultantly classifies their aggres-sion as predominately impulsive in nature (e.g., Helfritz & Stanford,2006; Stanford et al., 1997). The categorization was used to includeparticipants who demonstrated marked problems related to theirimpulsiveness evidencing a variety of outbursts not solely relatedto one social situation (e.g., relationships, school stressors, etc.).Age- and gender-matched controls reported no episodes of aggres-sion in the past six months and self-reported a score of 3 or less onthe Irritability subscale. The online survey also contained self-report measures to compare personality traits of the respectivesamples including the Buss-Perry Aggression Questionnaire (BPAQ;Buss & Perry, 1992), the Life History of Aggression Questionnaire(LHA; Coccaro, Berman, & Kavoussi, 1997) and the BIS/BAS Scales(Carver & White, 1994), along with substance use measures includ-ing the Alcohol Use Disorders Identification Test (AUDIT; Baboret al., 2001) and the Drug Abuse Screening Test (DAST-20;Skinner, 1982).

2.1.3. EEG and data reductionThose who met basic criteria for either the IA or control group

were invited to the lab for an in-person electroencephalogram(EEG). Subjects chose partial course credit or a $25 VISA gift cardas compensation for participation.

Physiological recordings were obtained between 3:00 and6:00 PM. Participants’ scalps were prepared with rubbing alcoholand a slightly abrasive gel (NuPrep) to increase scalp conduction.Their heads were fitted with a Neuroscan Quick-Cap with 64 tinelectrodes (International 10–20 system) with standard and inter-mediate positions, along with four eye electrodes measuring blinkand one on each mastoid for referencing. Participants sat in a pad-ded chair in a shielded and anechoic chamber during all EEGrecording. Resting EEG was recorded for eight minutes withone-minute blocks of eyes open (O) or closed (C) in one of two

Cohen’st(22) p d

�8.04 <.001 3.25�5.56 <.001 2.23�8.32 <.001 3.35�4.27 <.001 1.71�8.63 <.001 3.55

�9.61�3.31 <.001 3.84�5.43 .007 1.44�10.16 <.001 2.40

<.001 4.38

1.47 .156 0.600.90 .381 0.381.01 .326 0.423.39 .003 1.03

ression (LHA; Coccaro et al., 1997), Behavioral Inhibition Scale/Behavioral Activationscores on that measure than controls.

Left Right1.8

2.0

2.2

2.4

2.6ControlsIAs

Alph

a Po

wer

Fig. 1. Comparison of the interaction between hemispheres and group membershipat rest for Study 1. Note: Alpha power is inversely related to activity.

Table 2Group differences in self-report measures in Study 2.

Controls IAs a Cohen’sMeasure M (SD) M (SD) t(28) p d

BPAQPhysical 13.13 (2.53) 24.40 (5.88) �6.82 <.001 2.49Verbal 12.07 (2.76) 16.33 (4.99) �2.90 .008 1.06Anger 9.60 (1.35) 21.40 (5.14) �8.60 <.001 3.14Hostility 16.27 (6.26) 25.00 (6.97) �3.61 .001 1.32Total 51.07 (9.47) 87.13 (17.10) �7.15 <.001 2.61

LHAAggression 4.87 (3.82) 11.40 (4.67) �4.20 <.001 1.53Self-directed 0.07 (0.26) 0.80 (1.42) �1.96 .069 0.72Consequences 0.47 (1.06) 2.00 (1.41) �3.36 .002 1.23Total 5.40 (4.49) 14.07 (5.42) �4.77 <.001 1.74

BIS/BASBIS 17.33 (3.02) 20.80 (3.12) �3.09 .004 1.13BAS reward 16.27 (2.73) 16.40 (2.56) �0.11 .910 0.07BAS drive 11.20 (2.93) 10.67 (2.06) 0.58 .569 0.20BAS fun-seeking 11.07 (3.67) 12.13 (2.23) �0.96 .345 0.35

SPSRQSP 8.60 (3.89) 14.53 (4.14) �4.05 <.001 1.48SR 12.33 (3.75) 13.07 (4.30) �0.50 .832 0.18

Note. Buss-Perry Aggression Questionnaire (BPAQ; Buss & Perry, 1992), Life Historyof Aggression (LHA; Coccaro et al., 1997), Behavioral Inhibition Scale/BehavioralActivation Scale (BIS/BAS; Carver & White, 1994), Sensitivity to Punishment andSensitivity to Reward Questionnaire (SPSRQ; Torrubia et al., 2001). Negative tstatistics indicates IAs reported higher scores on that subscale than controls.

Left Right1.5

1.7

1.9

2.1

2.3 ControlsIAs

Alph

a Po

wer

Fig. 2. Comparison of the interaction between hemispheres and group membershipat rest for Study 2. Note: Alpha power is inversely related to activity.

S.L. Lake et al. / Personality and Individual Differences 70 (2014) 131–135 133

counterbalanced orders (OCCOCOOC or COOCOCCO) with a 15-sbuffer between blocks. A fast Fourier transformation (FFT) sepa-rated all artifact-free data into frequency bands with a Hammingwindow of 1 s and a 50% overlap. Average alpha power at each sitewas natural log transformed, with alpha power inversely related tocortical activity (Neuper & Pfurtscheller, 2001). Hemispheric asym-metry indices were calculated by region of interest (ln[right] –ln[left]) producing a hemispheric index similar to previousresearch (e.g., Coan & Allen, 2003). The simplicity of the asymme-try index aids in understanding the differences between groups butdoes not show contribution of activity in each hemisphere (forreview, see Allen, Coan, & Nazarian, 2004), thus in addition to ttests, a mixed-design ANOVA was computed with Region (mid-frontal [i.e., F3/F4], lateral frontal [i.e., F7/F8]) and Hemisphere(right, left) as within-subjects variables and Group (IA, control)as the between-subjects variable.

3. Results

We enrolled 26 participants in the study, but data from n = 2participants (both male IAs) were not included in analyses due tohead injuries previously undisclosed. A total of N = 24 participants(n = 14 women) were included in the analyses (n = 10 IAs). No sexdifferences were found between characteristics of interest, thussex was not included as a factor in the experiment. Comparingby group, IAs scored higher on most self-report measures of impul-sivity and anger compared to controls (see Table 1).

IAs had more right activity at a resting state than controls usingthe asymmetry index at both F3/F4 sites [t(22) = 2.365, p = .031,d = .84] and F7/F8 sites [t(22) = 2.743, p < .0001, d = .93]. Thesegroup differences also remained significant using a mixed-effectsANOVA as indicated by a Group X Hemisphere interaction[F(1,22) = 8.198, p = .009, g2 = .263], with more left alpha (and thusmore right activity) for IAs (MLeft = 2.23, SE = .06; MRight = 1.93,SE = .08) compared to controls (MLeft = 2.15, SE = .05; MRight = 2.46,SE = .07; see Fig. 1). The main effects between IAs and controls wererobust even after controlling for anger using the BPAQ Anger sub-scale [F3/F4 F(2,21) = 4.072, p = .032; F7/F8 F(2,21) = 4.992,p = .012] and impulsivity using the BIS-11 Total score [F3/F4F(2,21) = 3.859, p = .023; F7/F8 F(2,21) = 5.115, p = .034]. Examiningself-report measures revealed no statistical differences in three ofthe four BIS/BAS subscales (see Table 1), but controls scored higherthan IAs on BAS Fun-Seeking [t(22) = 3.39, p = .003, d = 1.03] sug-gesting they engage in more reward-seeking behavior than IAs.

4. Discussion

Study 1 showed IAs had increased right frontal cortical activityat a resting state compared to controls, even after controlling for

anger and impulsivity measures. Because emotional processingdeficits have been seen in other psychophysiological measure-ments of IAs, it seemed desirable to assess emotional processing.Therefore, Study 2 attempted to replicate Study 1’s results and fur-ther explore the nature of frontal asymmetry by introducing anaffective manipulation.

5. Study 2

5.1. Methods

Participants were recruited in the same way as Study 1, with atotal of n = 273 participants aged 18–27 completing prescreeningand n = 37 invited to the in-person EEG evaluation. Because menhave a higher tendency to display impulsivity in violent ways(Boyd, 2008; Coccaro et al., 1997), only men were included in thisstudy. A total of n = 34 men (Mage = 19.30, SD = 1.18) completedEEG recording. Along with the previous self-report measures, theSensitivity to Reward/Sensitivity to Punishment Questionnaire(SPSRQ: Torrubia, Avila, Molto, & Caseras, 2001) was included tomeasure individuals’ tendency towards BIS or BAS activity.

1.25

1.50

1.75

2.00

2.25 LeftRight

Rest Withdrawal Approach

Alp

ha P

ower

1.25

1.50

1.75

2.00

2.25 LeftRight

Rest Withdrawal Approach

Alp

ha P

ower

BA

Fig. 3. Comparison of alpha power between controls (A) and impulsive aggressors (B) for resting state, withdrawal imagery, and approach imagery. Note: Alpha power isinversely related to activity.

134 S.L. Lake et al. / Personality and Individual Differences 70 (2014) 131–135

5.1.1. EEGs and data reductionParticipants first underwent a resting EEG like Study 1. After the

resting EEG, two affective picture presentations were shown in arandom order. Each affective presentation consisted of 35 imagesfrom the International Affective Picture System (IAPS; Lang,Bradley, & Cuthbert, 2008). The two trials lasted approximately fiveminutes long, consisting of equally arousing withdrawal-(Mvalance = 3.69, SD = 0.93; Marousal = 5.88, SD = 0.77) or approach-(Mvalance = 7.12, SD = 0.50; Marousal = 5.52, SD = 0.92) motivated pic-tures chosen based upon the published ratings (Lang et al., 2008) ofarousal, positive valence, and dominance. Pictures eliciting with-drawal motivation included aggressive animals, mutilation, orthreat, whereas pictures eliciting approach motivation includedappetitive scenes such as a romantic embrace. Two separate EEGswere recorded with a 2-min resting period between the two affec-tive trials.

6. Results

From the N = 34 subjects who participated, three IAs and onecontrol were not included in the analysis (n = 2 lacked report ofphysical aggression during the intake interview, n = 1 left-handed[control], and n = 1 previous head injury). A total of N = 30(n = 15 IAs) comprised the final sample. IAs scored higher on mostself-report measures of impulsivity and anger compared to con-trols, and had more self-reported tendency to use the BIS (seeTable 2).

Replicating Study 1, IAs had increased right activity at rest usingasymmetry indices at F7/F8 sites [t(28) = 2.470, p = .020, d = .54]and F3/F4 sites [t(28) = 2.205, p = .034, d = .23]. These group differ-ences also remained significant using a mixed effects ANOVA asindicated by a Group X Hemisphere interaction [F(1,28) = 6.491,p = .017, g2 = .188]. A comparison of the means shows increasedleft alpha (and thus more right activity) for the IA group(MLeft = 2.04, SE = .06; MRight = 1.73, SE = .07) compared to controls(MLeft = 1.73, SE = .06; MRight = 1.88, SE = .08; see Fig. 2). Thesegroup differences remained robust even after controlling for angerusing the BPAQ Anger subscale [F3/F4 F(1,27) = 3.175, p < .05,g2 = .190; F7/F8 F(1,27) = 5.507, p < .01, g2 = .201] and impulsivityusing BIS-11 Total score [F3/F4 F(1,27) = 3.327, p < .05, g2 = .198;F7/F8 F(1, 27) = 3.092, p < .05, g2 = .186].

Using a mixed-effects ANOVA 2 (Group: IA, control) X 3 (Task:resting, withdrawal imagery, approach imagery) X 2 (Hemisphere:right, left) X 2 (Region: medial, lateral) factorial design with EEGalpha power as the dependent variable, there were significant taskand region main effects. However, because the interactions are ofinterest, the main effects will not be further discussed. There wasa significant Group X Task X Hemisphere interaction

[F(2,27) = 4.790, p = .016, g2 = .262], and further examinationshowed significantly more left alpha (and thus right activity) forboth IAs and controls during the withdrawal imagery. However,controls showed increased right alpha (and thus left activity) dur-ing the approach imagery while IAs did not (see Fig. 3). Controlsselectively engaged the BAS during the approach-motivated pre-sentation (more right alpha and thus more left activity) andengaged the BIS during withdrawal-motivated presentation (moreleft alpha and thus more right activity; see Fig. 3A), whereas IAsmaintained similar higher left alpha power (and thus more rightactivity) throughout all tasks (see Fig. 3B).

7. Discussion

The results of Study 2 replicated those of Study 1 by showingthat IAs had more right frontal cortical activity at rest than controlsand thus a tendency to use defensive approach, or approaching neg-ative stimuli. This result remained robust after covarying outimpulsivity and anger separately, suggesting trait anger and impul-sivity are not the underlying personality traits influencing thisfrontal lobe asymmetry in IAs. While viewing affective presenta-tions, controls were able to selectively engage the appropriatemotivational system dependent upon the emotional imagery.However, IAs showed an increase in right activity across all condi-tions and thus were unable to utilize different motivational sys-tems dictated by emotional cues.

8. General discussion and conclusions

Because controls were able to engage the BIS during with-drawal-related stimuli and the BAS in response to approach-related stimuli, one of two conclusions seems likely: IAs have anoveractive BIS with underactive BAS, or a normal BIS and underac-tive BAS. Given that BIS underlies the temperamental quality ofinhibition and pathological anxiety (Oosterlaan, 2001), this studylends evidence that the BIS is most likely overactive in those withimpulsive aggression (who thus lack the ability to inhibit coupledwith the tendency to use aggression in many situations). Indeed, acomparison between controls and IAs shows IAs have slightly moreactivity overall (not statistically significant, see Fig. 2). Due to thesmall differences seen between hemispheres, we do not haveenough power to conclude if IAs have an underactive BAS com-bined with an overactive BIS, or if the BIS overshadows a normalBAS. However, the trend seems to be in favor of an overactive BIS.

In line with Reinforcement Sensitivity Theory, IAs showed moreright activity and thus engaged the BIS more at rest compared tocontrols. Although controls could appropriately react emotionallyto stimuli, IAs were unable to engage the appropriate motivational

S.L. Lake et al. / Personality and Individual Differences 70 (2014) 131–135 135

systems providing evidence that impulsive aggression may be aconsequence of too much anxiety during neutral or non-anxioussituations (Perkins et al., 2007; Stanford et al., 1997). This maybe partly due to misappropriation of emotional resources similarto previous research (Conklin & Stanford, 2002). Additionally, thepersistence of right-sided asymmetry that IAs demonstrate maybe indicative of a predisposition to depression (Deldin & Chui,2005; Jaworska, Blier, Fusee, & Knott, 2012b). Although signs ofdepression or an anxiety disorder were exclusionary criteria, futurestudies should include self-report measures of depressive and anx-ious tendencies to clarify this result.

The current studies lend evidence towards recognizing restingand manipulated frontal lobe asymmetry as a marker for suscepti-bility to psychopathology, although the exact psychopathologyremains to be precisely identified. More right activity in IAs sug-gests those with an aggressive impulse control problem have diffi-culty recognizing or categorizing different types of emotionalstimuli and may then indiscriminately act out aggressively as aresult. Speculatively, impulsive aggressors may view many non-threatening situations as threatening, indicating a dysfunction inemotional processing resulting from an atypical biological system.This study adds to the growing body of literature that therapiesfocusing on helping impulsive aggressors change the way they pro-cess emotional information are likely the best way to reduceoutbursts.

Acknowledgments

The authors thank Brian Rundle, Mitchell Todd, and LindseyHicks for their excellent technical assistance.

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