Carlson, Joshua M

Greenberg, Tsafrir

Mujica-Parodi, Lilianne R

English

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Northern Michigan University NMU Commons Journal Articles FacWorks 6-2010 Blind rage? Heightened anger is associated with altered amygdala responses to masked and unmasked fearful faces Joshua M. Carlson joshcarl@nmu.edu Tsafrir Greenberg Lilianne R. Mujica-Parodi Follow this and additional works at: https://commons.nmu.edu/facwork_journalarticles Recommended Citation Carlson, J. M., Greenberg, T. & Mujica-Parodi, L. R. (2010). Blind rage? Heightened anger is associated with altered amygdala responses to masked and unmasked fearful faces. Psychiatry Research, 182(3), 281-3. DOI:10.1016/j.pscychresns.2010.02.001 This Journal Article is brought to you for free and open access by the FacWorks at NMU Commons. It has been accepted for inclusion in Journal Articles by an authorized administrator of NMU Commons. For more information, please contact kmcdonou@nmu.edu,bsarjean@nmu.edu. See	discussions,	stats,	and	author	profiles	for	this	publication	at:	https://www.researchgate.net/publication/44612388Blind	rage?	Heightened	anger	is	associated	withaltered	amygdala	responses	to	masked	andunmasked	fearful	facesArticle		in		Psychiatry	Research	·	June	2010DOI:	10.1016/j.pscychresns.2010.02.001	·	Source:	PubMedCITATIONS15READS1453	authors:Joshua	M	CarlsonNorthern	Michigan	University49	PUBLICATIONS			706	CITATIONS			SEE	PROFILETsafrir	GreenbergUniversity	of	Pittsburgh26	PUBLICATIONS			286	CITATIONS			SEE	PROFILELilianne	R	Mujica-ParodiStony	Brook	University84	PUBLICATIONS			1,119	CITATIONS			SEE	PROFILEAll	in-text	references	underlined	in	blue	are	linked	to	publications	on	ResearchGate,letting	you	access	and	read	them	immediately.Available	from:	Joshua	M	CarlsonRetrieved	on:	10	October	2016This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institutionand sharing with colleagues.Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third partywebsites are prohibited.In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further informationregarding Elsevier’s archiving and manuscript policies areencouraged to visit:http://www.elsevier.com/copyrightAuthor's personal copyBrief reportBlind rage? Heightened anger is associated with altered amygdala responses tomasked and unmasked fearful facesJoshua Michael Carlson⁎, Tsafrir Greenberg, Lilianne R. Mujica-ParodiDepartment of Biomedical Engineering, State University of New York at Stony Brook, Stony Brook, NY, USAa b s t r a c ta r t i c l e i n f oArticle history:Received 2 July 2009Received in revised form 19 January 2010Accepted 5 February 2010Keywords:AmygdalaAngerFunctional magnetic resonance imagingWe investigated anger-related variability in the BOLD fMRI response to crude/masked and detailed/unmasked fearful faces. Anger expression positively covaried with amygdala activation to crude fear, whiletrait anger negatively covaried with amygdala responses to detailed fear. This differential processing maytrigger aggression without the subsequent inhibition associated with distress cues.Published by Elsevier Ireland Ltd.1. IntroductionGiven the high incidences of aggression and violence that stemfrom the expression of anger, it is important to understand thefunctional neuroanatomy underlying individual differences withinthis variable. The amygdala is critically involved in the recognition offearful facial expressions (Adolphs et al., 1994), which are salientthreat and distress cues that are thought to reduce aggression/angerin healthy populations, thereby stabilizing social interactions (Marshand Blair, 2008). Aggression-related traits are associated withimpairments in recognizing fearful faces and hypoactive amygdalaresponses to fearful faces (Gordon et al., 2004; Marsh and Blair, 2008).In addition to emotion recognition, the amygdala is also involved inmodulating the expression of emotions, including anger (LeDoux,1996). Yet, the relationship between amygdala reactivity and thedisposition for aggressive behavior has not been examined.Evidence from animal (LeDoux, 1996) and neuroimaging (Liddellet al., 2005; Vuilleumier and Pourtois, 2007) research indicates thatthreat information is relayed to the amygdala through two pathways.These include a subcortical route (via the thalamus) for rapidresponses to crude threats and a slower cortical route (including thefusiform gyrus for visual stimuli) for more discriminative/detailedresponses. Here we investigated how amygdalar reactivity to bothcrude (initial sensory processing interrupted and restricted bybackward masking) and detailed (unmasked) facial cues is associatedwith trait anger (i.e., disposition to feel angry) and anger expression(i.e., disposition for aggressive behavior).2. Methods2.1. ParticipantsFifteen (female=7; 19–48 years old, M=26.60, S.D.=7.41) healthyconsenting adults participated in the study. Thirteen reportedbeing right-handed and two left-handed. Participants completed the State-TraitAnger Expression Inventory-2 (Spielberger, 1999) and the State-TraitAnxiety Inventory (Spielberger et al., 1970). Participants' Trait Anger (TA;11–23, M=14.8, S.D.=3.21), Anger Expression-Out (AE-O; 9–24,M=13.87, S.D.=4.09), and Trait Anxiety (20–41, M=32.33, S.D.=5.73) scores were within the normal range. TA and AE-O weresignificantly correlated with each other (r=0.66, P=0.008), but notwith age or Trait Anxiety (P'sN0.10).2.2. Experimental setup and procedureTheexperimentwas programmedand runwith E-prime (PsychologySoftware Tools, Pittsburgh, PA, USA). An MRI-compatible 60-Hzprojector with a 1024×768 resolution reflected stimuli onto a mirrorattached to the head coil. Facial stimuli (Gur et al., 2002) were grey-scaled and cropped to eliminate hair and other extraneous features.Each trial started with a 2300-ms fixation cue (+) centered on a blackbackground. Next, the initial face was briefly (33 ms) presented andthen immediately masked by a new face for 167 ms. Finally, a jitteredintertrial interval (M=5.5 s, 2.5–17.5 s) followed the face pairs. Trialtypes were determined by the order and expression of the initial face-mask face pairing, where masked fearful=fearful–neutral (FN),Psychiatry Research: Neuroimaging 182 (2010) 281–283⁎ Corresponding author. Laboratory for the Study of Emotion and Cognition,Department of Biomedical Engineering, Bioengineering Building, SUNY Stony Brook,Stony Brook, NY 11794, USA. Tel.: +1 631 632 1911.E-mail address: carlsonjm79@gmail.com (J.M. Carlson).0925-4927/$ – see front matter. Published by Elsevier Ireland Ltd.doi:10.1016/j.pscychresns.2010.02.001Contents lists available at ScienceDirectPsychiatry Research: Neuroimagingj ourna l homepage: www.e lsev ie r.com/ locate /psychresnsAuthor's personal copyunmasked fearful=neutral–fearful (NF), andneutral=neutral–neutral(NN). There were a total of 132 trials (44 of each type) presentedpseudorandomly in a 12-min run. The mask face was offset from theinitial face by approximately 1° of visual angle on either the Y- or X-axisto reduce apparent motion (Liddell et al., 2005). We do not claim thatbackward masking rendered the initial image subliminal per se, but itdid restrict fearful face processing during FN relative to NF trials.Participants were instructed to always maintain fixation in the centerof the screen and to pay close attention to the faces.2.3. Functional image acquisition and analysisA 3 T Philips whole body scanner was used to acquire 288 T2*-weighted scans with an EPI sequence using the following parameters:Repetition Time=2500 ms, Echo Time=22 ms, Flip Angle=83°, MatrixDimensions=96×96, Field of View=224×224mm, Slices=36, SliceThickness=3.5 mm, Gap=0. Standard preprocessing procedures wereperformed in SPM5, including image realignment corrections formovement, slice timing corrections, normalization to standard2×2×2mmMontrealNeurological Institute space, and spatial smoothingwith a Gaussian full-width-at-half-maximum 6-mm filter. First-levelsingle subject SPMs were created for each condition (FN, NF, and NN).Second-level analyses of FN vs. NN and NF vs. NN with TA and AE-Oregressors were created. Bilateral amygdala, thalamus, and posteriorfusiform gyrus (y≤−36) region-of-interest (ROI) analyses were per-formed in SPM5 using the Masks for ROI Analysis (Walter et al., 2003)with a cluster-level search volume corrected (SVC) α=0.05 and extentthresholds of 10 and 20 continuous voxels for subcortical and corticalregions, respectively.3. ResultsAs displayed in Fig. 1, the results of the ROI analyses revealed that formasked (FNNNN) fearful faces AE-O positively covaried with the leftamygdala (−26, 0, and −16, t(13)=2.92, Pcorrected=0.006, k=40),while for unmasked (NFNNN) fearful faces TA negatively covaried withthe right amygdala (28, 0, and −26, t(13)=2.20, Pcorrected=0.023,k=21). These associations remained significant (P'sb0.05) in partialcorrelations controlling for age, gender, and anxiety. There were nosignificant associations in the thalamus or posterior fusiform gyrus.4. DiscussionTo our knowledge, we provide the first evidence that individualshigh in anger expression have an amplified left amygdala response tocrude (i.e., backward masked) representations of fearful faces. Addi-tionally, we found that higher levels of trait anger coincided withdecreased right amygdala reactivity during unrestricted/unmaskedfearful face processing, which is consistent with previous findings ofhypoactive amygdala responses and impaired fearful face recognition inantisocial and aggressive populations (Gordon et al., 2004; Marsh andBlair, 2008). Anger expression and trait anger were not associated withactivity in perceptual areas (i.e., thalamus and fusiform gyrus), but onlyin the fear/emotion processing amygdala.Fig. 1. The left amygdala positively covaried with anger expression during crude/masked fearful face processing (left panels). The right amygdala negatively covaried with trait angerduring detailed/unmasked fearful face processing (right panels).282 J.M. Carlson et al. / Psychiatry Research: Neuroimaging 182 (2010) 281–283Author's personal copyThe observed hyperactive left amygdala response to crude fearexpressions in individuals with higher levels of anger expression mayreflect a mechanism that triggers aggressive responses, while thehypoactive right amygdala response to detailed fear expressions mayreflect deficits in fearful face processing, which result in dismissal ofthese distress cues. In extreme cases, this differential amygdalareactivity may lead to “blind rage” or aggressive behavior withoutappropriate distress processing and subsequent withdrawal. Interest-ingly, the observed amygdala asymmetries are consistentwithmodelsof affective asymmetry where the left hemisphere is thought to beinvolved in approach-related behaviors (e.g., lashing out), whereasthe right hemisphere is associated with withdrawal behaviors andnegatively valenced perceptual processing (Demaree et al., 2005).Given our sample size and lack of a recognition test, future research inthis area is needed. Nevertheless, the current findings lead us tospeculate that two processes are associated with aggression—a rapidreactivity to crude threat/distress that facilitates the aggressiveresponse and a deficit in processing detailed threat/distress cuesthat maintains it.AcknowledgementsThis research was supported by the Office of Naval Research#N0014-04-1-005 (LRMP) and the National Institutes of Health#5MO1-RR-10710 (General Clinical Research Center).ReferencesAdolphs, R., Tranel, D., Damasio, H., Damasio, A., 1994. Impaired recognition of emotionin facial expressions following bilateral damage to the human amygdala. Nature372, 669–672.Demaree, H.A., Everhart, D.E., Youngstrom, E.A., Harrison, D.W., 2005. Brain laterali-zation of emotional processing: historical roots and a future incorporating“dominance”. Behavioral and Cognitive Neuroscience Reviews 4 (1), 3–20.Gordon, H.L., Baird, A.A., End, A., 2004. Functional differences among those high and lowon a trait measure of psychopathy. Biological Psychiatry 56, 516–521.Gur, R.C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., 2002. A method forobtaining 3-dimensional facial expressions and its standardization for use inneurocognitive studies. Journal of Neuroscience Methods 115, 137–143.LeDoux, J.E., 1996. The Emotional Brain: The Mysterious Underpinnings of EmotionalLife. Weidenfeld and Nicholson, London.Liddell, B.J., Brown, K.J., Kemp, A.H., Barton, M.J., Das, P., Peduto, A., Gordon, E., Williams,L.M., 2005. A direct brainstem–amygdala–cortical ‘alarm’ system for subliminalsignals of fear. Neuroimage 24, 235–243.Marsh, A.A., Blair, R.J., 2008. Deficits in facial affect recognition among antisocialpopulations: a meta-analysis. Neuroscience and Biobehavioral Reviews 32, 454–465.Spielberger, C.D., 1999. State-Trait Anger Expression Inventory-2. PsychologicalAssessment Resources Inc., Lutz, FL.Spielberger, C.D., Gorsuch, R.L., Lushene, R.E., 1970. Manual for the State-Trait AnxietyInventory (Self-Evaluation Questionnaire). Consulting Psychology Press, Palo Alto, CA.Vuilleumier, P., Pourtois, G., 2007. Distributed and interactive brain mechanisms duringemotion face perception: evidence from functional neuroimaging. Neuropsycho-logia 45, 174–194.Walter, B., Blecker, C., Kirsch, P., Sammer, G., Schienle, A., Stark, R., Vaitl, D., 2003.MARINA: an easy to use tool for the creation of MAsks for Region of INterestAnalyses. Paper presented at the 9th International Conference on FunctionalMapping of the Human Brain, New York, NY.283J.M. Carlson et al. / Psychiatry Research: Neuroimaging 182 (2010) 281–283

Blind rage? Heightened anger is associated with altered amygdala responses to masked and unmasked fearful faces

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Blind rage? Heightened anger is associated with altered amygdala responses to masked and unmasked fearful faces

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