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12 A REVIEW OF SOCIAL NEUROSCIENCE RESEARCH ON ANGER AND AGGRESSION

Douglas j. Angus, Dennis j . L. G. Schutte~ David Terburg, jack van Honk, and Eddie Harmon-jones

Introduction

Responding aggressively to potential threa ts from conspecifics is, for man y

organisms, a highl y adaptive strategy to maintain we ll - being, soc ial dominance,

and resource access (Mazur & 13ooth , 199H; van H onk et a!., 200 I). H owever,

in modern humans, the adaptive value of rea c tive aggression is dimini shed , and

is often maladap tive. For in stan ce, excessive and uncontrolled anger and

aggressive actions (e.g., physical or verbal harm) are associated with a ran ge of

health comequen ces (13uck ley et a!. , 20 IS ; Mostofsky. M acl ure, ToAer, Muller,

& Mittleman. 20 13; Okuda et a!., 20 IS). Yet despite these negative outcomes,

reactive soc ial aggress ion is retained in humans, and conve rging evidence

suggests that its core me chani sm s are phylogeneti ca lly ancient and shared with

many non-human animals.

We distinguish between two subtypes of social aggression-proactive and

reactive aggression (va n Honk, H armon-Jones, Morgan , & Schutter, 20 I 0).

These two subtypes are use ful heuri sti cs rather than absolutes (Anderso n &

Bushman , 2002) that describe distin c t observable behaviors. Proactive aggression

is in strumental and pre meditated, and while associated with achieving a

particular goal, is not associated with goal frustration or perce ived threats. In

contrast, rea c tive aggression is not premeditated and involves anger and

responding to soc ial threa ts and fru strated goals.

We begin thi s review by discussing the evidence for the involvement of the

steroid hormon es testoste rone and co rrisol in guiding and executin g angry and

aggressive actions. Then we reca pitulate the core assumptions and theoretical

basis of th e Triple Imbalance H ypothesis, whi ch proposes that soc ially aggressive

act ions are underpinned by three interacting systems of the brain , and that :~1-.o l ~nrPs within these <v<tPm< ~ r" ~«nrio t Pcl with an increased proclivity to

224 Angus, Schutter, Terburg, van Honk, & Harmon-jones

act aggressively in response to perceived th reats and when seeking rewarding

stimuli (van Honk et a!., 201 0). Then we review recent research on reactive aggression which discusses the role that each of the th ree brain systems have

in motivating and facilitating reactive aggression. Finally, we discuss evidence

for the role of the corpus callosum in mediating imbalances in the most recently

evolved of these brain systems.

Core Brain Chemicals for Reactive Aggression

A promising approach to modeling neuroendocrine contributions to anger and

reactive aggression in humans has focused on the mutually antagonistic effects

of testosterone and cortisol (van Honk et al., 2010). In non-human species,

testosterone levels are reliably associated with increased aggression toward

conspecifics, and they predict sex differences in socially aggressive behavior

(Archer, 1988). In humans, greater testosterone levels have been found to predict

aggressive attitudes, with castration reducing their endorsement (Van Goozen,

Cohen-Kettenis, Gooren, Frijda, & Van De Poll, 1995). Moreover, situationally

increased testosterone levels in response to a laboratory anger induction predict

increased self-reported anger to the induction (Peterson & Harmon-Jones, 2012).

Additional evidence for the role of testosterone in shaping anger and aggressive

behavior in humans comes from a program of research associating testosterone

levels with observer-rated violence and aggressive antisocial behavior in male and

female prison populations (Dabbs, Carr, Frady, & Riad, 1995; Dabbs & Hargrove,

1997; Dabbs & Morris, 1990). Intriguingly, because of the putative mechanism

by which testosterone affects aggression, its effects may not be consciously

accessible or observed in self-report (van Honk & Schutter, 2007a). In contrast

to testosterone, cortisol has been associated with a reduced tendency to engage

in aggressive behaviors . Lower levels of cortisol are observed in populations at

risk of violent antisocial outbursts and children with socialization problems

(McBurnett e t al., 1991; Vanyukov et al., 1993).

Several properties of the endocrine axes that produce testosterone and

cortisol are of particular importance with respect to their role in motivating

and guiding aggressive behavior. First, the hypothalamic-pituitary-gonadal

(HPG) and hypothalamic-pituitary-adrenal (HPA) axes-which synthesize

testosterone and cortisol respectively-are mutually antagonistic (Viau, 2002).

TestOsterone has been shown to inhibit stress-related responses in the HPA

(Viau, 2002), while cortisol-and its analogues in other mammals-has been

shown to inhibit the release of testosterone and the action of testOsterone at

target sites (Johnson, Kamilaris, Chrousos, & Gold, 1992; Til brook, Turner, &

Clarke, 2000). Second, testosterone and cortisol have distinct effects on the

amygdala, with the former promoting vasopressin gene expression and approach

behaviors (Schulkin, 2003), and the latter promoting corticotropin releasing

hormone (CRH) gene expression and withdrawal behaviors (Schulkin, 2007).

The opposing effects of testosterone and cortiso l arc also observed at a psychobiological level in many species. Testosterone has been found ro increase

approach behavior, including aggression and reward sensitivity (Carr, Fibiger,

& Phillips, 1989), while also reducing withdrawal behaviors, fear, and punish­

ment sensitivity (Hermans, Putman, 13aas, Koppeschaar, & van H onk, 2006).

Research using the low.1 Gambling Task (13echara, Damasio, A. 1\.., Dama.,io,

H., & Ander'>on. 199~) has found testosterone administration to increase

sensitivity to reward. Clll'>ing indi\·iduab to m .1ke more ri.,ky .llld di.,ad\·,uHJ­

geous choices (van Honk et .1!.. 200~) . CorrebtiollJI findings ~ugge'>t thJt

corti-,ol ha., tht· oppo.,ite etTen. with more .1dvanr.1geom choice'> m.JLic by

individual'> with high corti.,ol ln·e!., .llld more di.,.Jdv.lllt.Jgeou-, choice., made

by mdi\·idu .d., \\·ith low corti..,ol lc\·els (\',111 Honk, Schutter. Hnm.1m. &

Putman. 2003) . Rather th.1n eithL'r one of the'>e hormone'> being .,ingularly respomiblc for

.Jggres,ive tendencie'>, the imbJLJnce bet\\·een te'>to'>tcrone .md corti.,ol i, pivoul

(van Honk et al.. 20 I !l) . The tinding'> of 'e\·eral studie'> that included me.J'>ure'>

of both te'otmterone .llld cortisol .JrL' particuL1rly reve.11ing. and provide critical

.,upport for thi, hypothesis. FiP,r. 0\'ert .Jggre ... ,ion in adolc-,cem nulc., i'>

predicted b\· high testo'>terone only in tho'le \\·ho abo ha\'L' lo\\' corti.,ol lcveb

(Popma et .d .. 2!Hl7) . Second, girl'> with conduct di.,order h.l\'e been found to

h.J\'l' gre.Her te'>tmterone Jnd lower cortisol leveb (Pajcr et .11., 2!Hl(>) . Third,

rc'oe.Jrch examining the contribution'> of te'>to'>terone and corti'>ol to rc.1ctive

.Jggn:,sion and dominance indicated that te'>tosterone predined increa.,ed

.1ggre.,.,ion in m.Jic., and fem.Jlc'>, but only in tho,e with lo\\' corti'>ol. High lc\·eJ..

of corti'>ol may even reverse the ctTects of te'>to'>terone, \\·ith less .1ggre'o'>ion and

dominance ob.,erved in high-cortisol, high-te'>tosterone '>ubject'> (Meht.l &

Joseph>. 20 I !l) . lntere'>tingly. both proactive and reacti\·e .Jggre'>'>ion have been ,J'I.,ociated

with b.Js.d testostnone .llld cortisol lcveb in oppo.,itL' way'>, and there i'> evi­

dence th.H the mono.unine serotonin is p.lrticularly important for di'>tingui.,h­

ing between the>e aggression subtype> (van Honk & Schutter, 2006b) . Lo\\'

'>eroronin lc\·eb in individuab \\'ith high te'>tO'>tcrone and low corti'ool

leveh m.1y predict their proclivity ro rc>pond with reactive aggre.,.,ion (Miczek

et .1!.. 2007) . Although the mechanisms that link '>eroronin .md the '>teroid horn1one'>

te'>tO'>terone .1nd cortisol are not well under'>rood, there i'> .Jbund.uH e\·idence

for the cxi.,tence of bidirectional relatiomhip., between .,erotonin and the

'>teroid hornwne'> testosterone and corri-,ol. Te.,tmterone h.h .Jntagoni'>tic

effect'> on .,eroronergic function, while low '>eroronin .lppe.Jr'> to prcdi..,pme

individu.d-, row.1rd reactive aggres>ion in high te'lto'>terone co1Hext., (13irger

et .1!.. 2003) . Although low se rotonin enhance ... withdr,I\\',JI- and .lppro.lch­

reLncd bch ,l\'iors-fear and social aggres'>ion- te'>tO'>tl'rone block'~ the etTen

of the former (Kuba la, McGinn is, Anderson. & Lumia. 2008) . Low .. erotonin

may shift aggression-related motivations toward a fearful-defensive form of reactive aggression (van Honk et aJ., 2010).

Interestingly, cortisol and its analogues differentially augment the inhibitory effects of serotonin. While high cortisol levels are associated with reduced aggression , low levels are associated with a dampening of serotonin function, and increased aggression in response to stress (C. H. Summers & Winberg, 2006; T. R . Summers et al., 2003). During stress-related aggressive acts,

increased cortisol and serotonin levels serve to inhibit the escalation of further

aggression; when the cortisol and serotonin response does not occur, aggressive acts are longer and more intense (T. R. Summers et al., 2003).

The Triple Balance Hypothesis

Before discussing the Triple Imbalance H ypothesis and supporting research, it

is necessa ry to detail its conceptual and theoretical foundations and core

assumptions. These are primarily derived from the Triple Balance Hypothesis

(TBH), which proposes that the survival and well-being of social animals is

dependent on the selection of appropriate responses to rewarding and punishing

features of their environment (van Honk & Schutter, 2005, 2006b). These

responses can be conceptualized as being either approach- or withdrawal­

related actions, and a balance between these different motivational directions

is critical for the well-being of individuals and groups (Ressler, 2004).

Building on previous neuroanatomical and biological frameworks and

theories that utilize an evolutionary approach to explaining their respective

phenomena (Jackson, 1887; MacLean, 1990), the TBH is organized into three

interacting and phylogenetically distinct biobehavioral balances. The oldest level

of this model is the subcortical balance, wherein testosterone and cortisol shape

approach- and withdrawal-related actions and facilitate their execution (va n

Honk et al., 2010). Moreover, testosterone and cortisol have differential effects

on behavior and on subcortical regions that comprise the brain 's defense circuits

(e.g., the amygdala , hypothalamus, and brain stem; Blair, 2004; H ermans, Ramsey,

& van Honk, 2008).

The next most recent level is the top-down cortical control of subcortical

regions via the prefrontal cortex (PFC). The evolution of the PFC-beginning

approximately 200 million years ago-allowed for the regulation of subcortical

drives by the increasingly complex PFC, with the degree of regulation

depending on subcortical-cortical balance.

Finally , in humans and non-human primates, the PFC has become

increasingly specialized, with systems associated with approach- and withdrawal­

related processes lateralized to the left and right hemispheres (Harmon-Jones

& Allen , 1998; Hortensius , Schutter, & Harmon-Jones, 2012; Kalin, Larson ,

Shelton, & Davidson, 1998). These often competing and mutually inhibiting

systems in the left and right PFC constitute the cortical balance .

The Triple Imbalance Hypothesis

The Triple Imbalance Hypothesis (TI H) is focused on the three interacting and phylogenetically di stinct brain systems that motivate and facilitate moving toward or moving away fi·om stimuli as proposed in the TBH (van Honk et al., 201 0). These systems are tho ught to underpin flexibl e and adaptive responding in contexts that may require approac h-rela ted (a nge r and aggression) or withdrawal-related (fea r and submiss io n) responses. The TI H posits that

imbalances in these systems are predictive of an increased or decreased tenden cy

to engage in reac tive soc ial aggression. Testosterone and cortiso l have powerful

neurochemica l effects that progress from their subco rti ca l amygda la-ce ntered

sires of act ion and influence the perceptio n of and respo nse to potential threats.

In this context, the un consc ious perception and eva luation of fac ial expressions

of anger is of part icular importance. In humans, angry faces se rve as threa t signals

in soc ial dominance contexts, with extended gaze and eye contac t (e.g., vigil ance)

indica ting that the facial expression is automati ca lly evaluated as a dominance

challenge, and expressing a willingness to confro nt this chall enge. In contrast,

rapidl y ave rrin g one's gaze is submissive, de-escalating aggression between both

parri es (Mazu r & Booth , 1998). That is, angry faces ca n produce either an

aggressive dominance response or a fearful submission response in individuals

(van H onk et al. , 2010; van Honk & Schutter, 2007a). The extent to which these vigi lance and .!voidan ce res po nses re fl ec t

dominance and submission motivations, their relati o nship with o ther aggressive

tendencies, and their subcortical and cortical underpinnings have been examined

in a progr.1m of research. This research , and assumptio ns regarding the automati c

e\·aluarion of angry faces, forms the basis of empiri ca l res ts of th e TIH . 13elow,

we review evidence regarding imbalances at each le vel of the TI H .

Subcortical Imbalances

Evidence for a ~ubcortical imbalance model of reactive aggression came from

early studi es which showed that a high testostero ne and low cortiso l ratio wa<;

correlated with in creased vigilance toward angry faces in emotiona l Stroop

tasks (van H onk et al., 1998, 2000; van Hon k et al. , 1999) . As no ted above.

increased vigil ance roward angry faces is thought to refle ct an approach- related

and aggressive do minance response, an interpretation that is cons istent with

past research showing that high testosterone is associated with soc iall y domi­

nant attitudes and low cortisol with ami-social attitudes (van Honk & Schutter,

2006b). There is also direct evidence for the en hancin g effect of tes tosterone on

social aggress io n. In a double-blind placebo-contro ll ed study, yo un g female

participants passively viewed faces with angry, happy, o r neutral expressiom while pulse rare was measured via finger plethysmograph. Th ese pulse data

were used to quantify the cardiac defense response (CDR), a phasic stimulus­driven increase in heart rate indicating preparation of flight or fight (Ohman, 1997) . T estosteron e administration was associated with greater CDR in response to angry face s, but not to happy or neutral faces (van Honk et al., 2001 ). Because testosterone inhibits fear and avoidance responses, the CDR potenti ati on defensibly refl ects an increased tendency to respond to angry faces with dominance and aggression (Hermans et al. , 2006; van Honk, Peper, &

Schutter, 2005). R ecent resea rch suggests that the aggression-enhancing and fear-reducing

effects of testosterone may have t\vo distinct neurochemical mechanisms (Terburg

& van Honk , 2013). Although pas t studies have shown testosterone administra­tion increases the blood-ox')'gen- level-dependent (BOLD) signal in regions that comprise the subcortical reactive aggression system (Blair, 2004; Hermans et al.,

2008), recent resea rch sugges ts g rea ter specifi city in the neurochemical

mechani sms and behavioral consequences at the level o f the amygdala. In addition to increasing aggressive vigilance via the upregulati on of vasopressin

gene expression in the central-medial amygdala (CMA), testosterone may also

increase the inhibition offear vigilance via more ve ntral regions of the amygdala like the basolateral amygdala (BLA). R ecent studi es suggest that lesions to the

BLA are associated with enhanced vigil ance toward faces expressing fear

(Terburg, Morgan, et al. , 2012), and increased attention toward fri ghtened body postu res (De Gelder et al. , 2014) . U sing th e same experimental model,

testosterone administration has indeed been found to decrease vigilance to faces expressing fear (van Honk et al. , 2005).

Importantly, the effects of testosterone on social aggression and dominance responses occur without consc ious awareness, without voluntary control of aggressive behavior, and without subj ective feelings associated with approach

motivation . Instead , the enhancement o f threat perception and motivation to respond with aggression by testosterone is non-conscious and automati c (van

Honk et al. , 2005). Previous studi es have reported that patients with extreme, uncontrollable outbursts of reactive aggression (Intermittent Explosive Disorder

[lED]) have diffi cul ty consciously recognizing angry fac ia l expressions (Best, Williams, & Coccaro, 2002), a fi nding that seems at odds w ith the vigilance­

enhancing effects observed elsewhere (van H onk et al. , 1999). Testosterone

appears to inhibit the consc ious recognition of ange r (van H onk & Schutter, 2007a), while enhancing no n-consc ious reac ti vity and dominance-related

behaviors. Empirical support for the unconscious-conscious distinction also

comes from recent studies examining the effect of testosterone administration on gaze fixa tion and saccade latencies away from eye contac t with angry faces (Terburg, Aarts, & van Honk, 2012). Unlike previous emotional Stroop tasks,

w hich required parti cipants to name the colo r of each stimulus (e.g., van Honk et al. , 1998, 2000; van Honk et al. , 1999), the eye-tracked gaze aversion task requires participants to use saccades away from the eye region of the face stimuli

to indicate their response (Terburg, Aarts, et al. , 2012; Terburg, Hooiveld , Aarts, Kenemans, & van Honk, 20 11 ), with more rapid saccades refl ecting enhanced gaze aversion . Administration of testosterone was found to reduce gaze ave rsion from angry faces, with greater saccade latencies compared to parti cipants given a placebo. Moreove r, the administration of tes tostero ne did no t influence parti cipants' subjective sense of dominance or aggression (Terburg, Aarts, et al. , 2012). Previous research has also found that saccade latencies are related to self­repo rted dominance (as assessed by the dr ive and reward-seeking subscales of the BAS; Carve r & White, 1994), suggesting that the eye-tracked gaze aversion tas k prov ides an index of dominance moti va ti ons (Terburg et al. , 20 II ) . Importantly, recent work shows that dominance motivation is only assoc iated with gaze ave rsion w hen the emo ti ona l content of stimuli is successfully masked,

supporting the interpretati on that these processes are unconsc ious and automati c

(H ortensius, va n Honk , de Gelder, & Terburg, 20 14). Alth ough tes tos tero ne- co rtiso l imbalances do appea r to produce quite

di ffe rent effec ts on unconsc ious and consc io us aggression- rela ted processes, can

this be unde rstood in terms of the brain mechan isms responsible' W e discuss

this question below .

Cortical-Subcortical Imbalances

The influence of testos tero ne and cortiso l on th e process ing of moti va ti onall y

releva nt stimuli occ urs at multiple leve ls. N o t onl y do these stero id hormones modulate ac tivity at subcortica l levels (e.g., in th e amygdala), but th ey also

alter communi ca tio n between subcorti ca l and co rti ca l reg ions, w hich may give ri se to di ffe rences in the processing of angry faces and in th e regulati on

o r dysregulati o n o f reac ti ve agg ressio n act io ns. Th e bidirec ti o nal coupling

betwee n key subcorti ca l and co rti cal reg ions is instrumental fo r the to p-down cogniti ve regulati on behavior (Krin ge lbac h & R olls, 2003; R eiman, 1997; va n H o nk et al. , 2005), as well as the rapid feed ing fo rward of bo tto m- up impulses fro m the subcortex (Mo rris, Ohman, & Dolan, 1999). In parti cular, the rapid

process ing of soc ially threa tenin g stimuli by the amygdala may be fe d fo rwa rd to th e o rbital frontal cortex (OFC), where slowe r and higher- leve l emotional

processes occ ur (R eiman, 1997; va n H onk et al. , 2005). Testosterone has been found to reduce subcorti ca l- corti cal connec tivity. In

o ne fun cti o nal magneti c resonance imag ing (fM Rl ) stud y, testos tero ne

administration was found to reduce fun ctional connectivity be tween the O FC and the amygdala (van Winge n, Mattern , Yerkes, Buitelaa r, & Fernandez, 20 I 0). Intriguingly, individuals with lED do not show the sa me increases in corti ca l­subcortical coupling that are obse rved in contro l pa rti cipants when viewing angry faces (Coccaro, McCloskey, Fitzge rald, & Phan, 2007) , suggesting that dysfun ctional communication between these levels predi cts excess ive reactive

aggress ion (va n Honk et a!. , 201 0). Th e importance of co rti co-subcorti ca l

230 Angus, Schutter, Terburg, van Honk, & Harmon-jones

cross-talk in anger and aggression is supported by recent diffusion tensor imaging

(DTI) findings demonstrating that lower white-matter striatal-frontal cortical

con nectivity is associated with more aggressive behavior and impulsivity in

healthy volunteers (Peper, de Reus, van den Heuvel, & Schutter, 2015; Peper

et al., 2013). This association was m ediated by endogenous testosterone levels,

providing a possible neural mechanism for the relation between testosterone and

app roa ch-related behavior (va n Honk et al., 2010).

Communication between subcortica l and corti ca l regions can also be

observed in the electroencephalogram ([EEG]; Schutter, Leitn er , Kenemans ,

& van Honk, 2006), with co uplin g be tween slow frequencies (delta , 1-4Hz)

localized-in part-to regions of th e subco rtex; and faster frequencies (beta ,

12 .5-30 Hz) localized to the PFC (Velikova et al., 2010). Consistent with fMRI

data, coupling be tween delta and be ta frequencies has been shown to decrease

with th e administration of testosteron e (Schutter & van Honk, 2004; van Honk

et al., 2004). In contrast, cortisol administration is associated with enhanced

conn ectivity (van Peer, Roelofs, & Spinhoven, 2008). Endogenous testosterone

is similarly co rrelated with reduced delta-beta couplin g (Miskovic & Schmidt,

2009). R esearch also suggests that delta-beta couplin g is correlated with individual

differences in dominance attitudes , and is inversely correlated with increased

vigilance to angry faces (Hofman, Terburg, van Wielink, & Schutter, 2013).

We argue that co rtical-subcorti cal connec tivity is criti ca l for th e generation

of socially appropriate responses to envi ronmental features that co11/d produce

reactive aggression. When th e subco rtex is decoupled from corti cal control

regions, individuals are more likely to respond in a largely disinhibited fas hion .

That is , activation in th e subco rtex m ay predispose individuals to respond

aggressively when th ere is a co ncomitan t reduction in top-down regulation by

cortical structures, with testosterone and cortisol biasing subcortical ac tivity and

cortical-subcortical coupling. Importantly, th e two hemispheres of th e frontal

cortex are functionall y heterogeneo us; th e left frontal cortex is associated with

approach motivation , while th e right frontal cortex is associated with withdrawal

motivation (i.e., the motivat ional direction model; Harmon-Jon es, 2003,

2004). As discussed in th e following section , this co rTical i111bala11ce has implications

for th e proclivity to engage in soc ial aggression .

Cortical Imbalances

Empirical support for th e motivation al direc tion model has bee n gathered using

different techniques in bo th healthy and cli ni cal populations, showing th at th e

left frontal co rtex is assoc iated with processes related to approach motivation,

while th e right frontal cortex is associated with processes related to avo idance

motivatio n (Amodio, Devine, & H armon-Jon es, 2008; H armon -Jon es, 2003;

H armon-jon es, Gable, & Peterson, 201 0; H arm on-Jones, E. , H armo n-Jon es, C., Serra, & Gable, 2011; H armon-Jones, Lueck, Fea rn , & H armon-Jo nes, 2006;

Research on Anger and Agg ression 231

Schutter, De Weijer, Meuwese, Morgan , & van H onk, 2008; Smith & Bell , 20 I 0;

Ve ron a, Sadeh, & C urtin , 2009). Behaviora l provocatio n swdies have found positive cor relati o ns between left frontal co rti ca l act ivati o n , app roach- rel ated

m otiva tion, and anger (H arm on-Jones, 2003; H armon-Jones et al., 20 I I ;

H armon-Jones & Sige l m an, 200 I) . Also, naturall y occurrin g re sting state

asymmetries in frontal electrica l osci llation., and corriul excitabi lity have been

shown to correLue with indi vid ual Ji!Terence; in approach- and .wo idan ce­

related motivation in healthy young adult'> (Schutter et al. , 200H). Left-'>ided

frontal electric corric1l asymmetries h.we also been found within th e

psychop.H hic population and in impri .,oned violent otTende r'>, providing .1

neur.1 l co rrelate th.H co uld exp lain th e .!pproach- motiv,Hion-re!Jted lifestyle of

these indi\'iduah that include., -,ema tion seeking, ri sk taking, and .Jggre'>'>ion

(H echt, 20 II; Keune e t al.. 20 12). R ecent e\' idence ; ugges ts that resti ng '>t.He

electric ,JsymnJetrie ., re co rded o\'er rhe ce ntral .,calp locatiom are more close ly

linked ro re'>pome inhibition, where.1s .1symm errie., over th e ,mterior regiom of

rhe .,c,tlp are more clo.,cly linked ro aggres\i\'C beha\'ior (H otinan & Schutter,

20 12).

Furthermore. frontal electric cortical .1symmerries have been found in young

infanr'> and ho ld predictive value. For insr.mce. '>t.lble left-sided electri c ti·onral

a .. ymmerrie., in int:mts at 10 and 2-t month ., of.1ge predict externa li zing behavior

as refk cred by approach m oti va tion and aggre'>'>io n , whereas righr-., ided fronral

J'>YIIIIlll'tric., predict internalizing beha\·ior a'> re flected by .!voidance moti\',Hion

,1nd .mxiery when ch ildren were 30 m onth., of age (Smith & Bell , 2010). Other

re'>ulr., ha\·e .,hown that a rightward fi·onral .l'>Y lllllletry incrc .J'>es the likelihood

of de\'Cioping ti.nure depressive symp to ms (Nmslock er al., 2011 ). A leftward

ti-ont,J l co rti ca l asymme try is, in turn , predicti\·e for the conversion lr0111 bipoL1r

II to bipolar I di.,order ove r a -t. 7 yea r follow- up. Thc.,e Lmer tinding'> co ncur

with beha\'ioral approac h-system hyper'>emiriviry modcb stating rlut tr.Jit

hype r'>cmiti\· iry to ap proac h m o ti va ti on and reward may predispme ro

hypomani c and manic states as refl ected by ti·onul co rti ca l a;ymmerry (Nm., lock

er al .. 20 12). U sing fMR. l , resea rchers fo und incn:.1ses of blood Row in the lcti:,

as compared to rhe right, dorsolateral prefronral co rtex during appro.Jch-rcLHed

goa l pur.,uit. and rhar this increase was pmiti\'cly correlated ro trait appro.Jc h­

moti\'ation (Berkm an & Liebe rman , 20 I 0). Moreover, an I ll C lraclopride

positron emission tomography (PET) study found rhar reLHi\'L' lcti: ao;yn1m errie.,

in '>tri.na l dopaminergic ac tivity w ere associated with a higher le\·el of approach

motivation (T o m<.:r , Go ldstein , Wang, W ong, & Volkow, 200H). The'le dau

nor only ind ica te that hemispheri c asymmetric<; .ne pre'>eiH on rhe '>Ubcortical

level, bur abo suggest reciproca l corri co-striata l- rhaL!mo-corri ca l imnacriom.

Additional evide nce for the frontal latera li zarion model of moti\',Hion and

emot io n hJ'> bee n provided by studies dep loying reperiti\'e rramcranialmagneric

.,ri mularion (rTMS) tO transiently interfere with ti·onul corric.1 l ltll! Ctioning. In

o ne '>t udy, inhibitory rTMS to the ri ght fi-onral co rtex , c.1ming a leti:ward

d>yuuucrry, resUiteo m more vigilant responses to angry faces. This vigilant response was suggested to be a result of increased approach motivation. In contrast, inhibitory rTMS to the left frontal cortex, causing a rightward asymmetry, resulted in attention directed away from angry faces (d' Alfonso, Van

Honk, Hermans, Postma, & De Haan, 2000). In a follow-up rTMS study, attention to angry facial expressions in a memory task was found to be reduced

following disruption of the left frontal cortex, as compared to disruption of the

right frontal cortex or sham (van Honk & Schutter, 2006a). Several other studies

have shown that inhibitory rTMS to the right prefrontal cortex increased risk­

taking behavior, decreased responsivity to faces expressing fear, and increased

left-sided EEG theta activity (Knoch et al., 2006; Schutter, van Honk, d'Alfonso,

Postma, & de Haan, 2001; van Honk, Schutter, d'Alfonso, Kessels, & de Haan,

2002). These findings ca n be interpreted as shifts in hemispheric balance

wherein vigilant and avoida nt responses to angry facial expressions uncover

motives for aggressive approach and anxious avoidance, respectively (van Honk & Schutter, 2007b).

Transcranial direct current stimulation (tDCS) was applied to examine the

interrelations between left-sided cortical asymmetry, anger, and aggression

(Hortensius et al., 2012). Individuals received insulting interpersonal feedback

following 15 minutes of tDCS to the frontal cortex and were allowed to

express aggression by administering noise blasts to the offending participant.

Individuals who underwent tDCS to increase relative left-frontal cortical

activity displayed more aggression as a function of their angry state. No such

relation between anger and aggression existed following increases of relative right-frontal cortical activity or sham stimulation.

The study by Hortensius et aJ. (201 2) suggests that environmental factors may

play a role in whether relatively greater left frontal activity results in a positive

versus negative approach. This notion finds additional support from other prior

studies that used unilateral hand contractions to evoke relatively greater left

frontal activity which caused greater positive affect in a positive situation

(Harmon-Jones, 2006), but greater negative affect/aggression in a negative

situation (Peterson, Shackman , & Harmon-Jones, 2008). Furthermore, individual

differences may influence these associations in a similar manner. Individuals high

in anger may often show greater left frontal cortical activity associated with

negative approach-related motivation , whereas optimistic individuals may often

show greater left frontal cortical activity associated with positive approach. Future

research is necessary to test this speculation. However, it is important to recall that

positive approach has been found to increase the likelihood of negative approach

under some conditions and vice versa (Angus, Kemkes, Schutter, & Harmon­Jones, 2015; Harmon-Jones & Peterson , 2008).

The present discussion of cortical asymmetries of motivational direction

revolves around the idea that approach and avoidance motivations are mutually

exclusive constructs at the conceptual and neural level. Past research has suggested

that externalizing (e.g., aggression) and internalizing (e.g., anxiety) problems may coexist for some individuals (Lara, Pinto, Akiskal, K. , & Akiskal , H., 2006). These problems are often found to coexist at the trait level of analysis by summing behavioral responses over many discrete states. It is thus possible that in a specific

episode or state (that may only occur for a few milliseconds), approac h (or avoidance) motivation may dominate the system and suppress avo idance (or

approach) motiva tion . Such a notion would be consistent with the idea that in a

given situation , the organism needs to respond with approach or avoidance when

confronted with biologically sign ifi cant stimuli. Alternatively, anger and aggression

have been interpreted as ways of copi ng with anxiety. From this point of view,

anger and aggressive behavior can be considered secondary to the primary

motivational tendency associated with anxiety which is avoidance. Furthermore,

it has been extensively shown that anxiety has a stron g subcorti ca l basis (e.g., the

amygdalar-septo- hippocampal complex) which together with a naturally left­

biased frontal asymmetry may nonetheless result in approach-related behavior. In

theory, this interpretation cou ld also explain aggression resulting from defensive

motivation that is rooted in fear rather than .1nger. We specul ate that during

highly aversive situations, the fight-flight system (Gray & McNaughton , 2003)

can be shifted toward "'fight" rather th an '" flight," wherein the subcortical fear

circuit ac tivates the naturally left-b iased approach system paralleled by ca llosa l

inhibition of the avoidance system.

Cortical Imbalances and the Corpus Callosum

Cortical asymmetries may reflect differences in reciprocal interactions between

the hemisp heres. Anatomical connections between the he misp heres ,1re

established through the corpus callosum which is exclusively found in placental

mammals. The corpus callosum is th e largest white-matter fiber tract in the

human brain, comprised of200-300 million fibers which are coa rsely organized

in a topographical fashion (Aboitiz & Monti el, 2003). The majority of ca ll osa l

projections are homotopic in nature, connecting equivalent regions between

the two hemispheres. The anterior third of th e corpus ca llosum, term ed the

genu, links the prefrontal cortical hemispheres and the ante rior c in guli .

The rostral part of the callosal body (trun cus) links the motor areas, whereas

the middle part of the central body interconnects the sensorimo tor and audirory

areas. Finally, the posterior parts of the corpus ca llosum link the temporoparietal

cortice'> (isthmus), and the most caudal parr of the posterior corpus ca llosum

(splenium) connects the occipital hemispheres (Pandya & Seltzer, 1986). The

composition of commissural fibers varies across the severa l parts of the corpus

ca llosum : Poorly myelinated small-caliber(< 2 ~1m in diameter) slow-condu cting

tlbers connec t the temporal, parietal, and frontal cortices; while highly

myelinated large-ca liber (> 3 ~1111 in diameter) fast-conducting fibers arc most

dense in con nections between the hemispheres of the pre motor, sensorimotor,

and occipital regions. It is generally assumed that the slow-conducting fibers support higher-order processes, whereas the fast-conducting fibers are necessary for midline fusion in the sensory domain. The corpus callosum plays a key role in the processing of the input and output signals of each hemisphere that is necessary for effectively coordinating thought and behavior (Nowicka &

Tacikowski, 2011 ). The cerebral hemispheres operate as semi-independent

parallel processing systems, and the inhibitory pathways of the corpus callosum

are assumed to be essential for interhemispheric signal transfer and

communication (van der Knaap & van der Ham, 2011).

Even though the role of the corpus callosum in aggression has been debated

for several years, the idea of commissural abnormalities relating to aggression

obtained a more firm empirical basis after reports of abnormal functional

cortical asymmetries and reduced interhemispheric electrical signal coherence

in violent patients diagnosed with antisocial personality disorder (Flor-Henry,

Lang, Koles, & Frenzel, 1991 ). Additional support for the callosal dysfunction

theory of aggression was provided by a positron emission tomography (PET)

study showing reduced metabolism in the corpus callosum of murderers

pleading not guilty by reason of insanity (Raine, Buchsbaum, & Lacasse, 1997).

Structural white-matter abnormalities in the corpus callosum have also been

verified in psychopathic individuals as compared to controls; and a dimensional

parametric analysis showed that the callosal aberrations correlated to antisocial

behavior and low autonomic activity (Raine et al., 2003). The observed

increased callosal volumes and fiber length in this study were explained by

possible neurodevelopmental problems associated with reduced axonal pruning

of excitatory commissural fibers.

Other evidence in support of callosal involvement in aggression comes from

recent studies using transcranial magnetic stimulation (TMS). Transcranial

magnetic stimulation technology provides a unique way of measuring effective

connectivity between the hemispheres by assessing signal transfer and

transcallosal inhibition i11 vivo (Ferbert et al., 1992). Transcallosal inhibition

(TCl) is based on excitatory callosal fibers targeting inhibitory interneurons on

the homotopic area of the contralateral hemisphere . When the primary motor

cortex is exposed to a strong but short-lasting electromagnetic pulse, the

induced electric current in the brain will activate cortical pyramidal neurons

causing a contralateral muscle twitch of, for example, the abductor pollicis

brevis. The amplitude of this twitch is called the motor evoked potential (MEP).

Transcallosal inhibition can be demonstrated by comparing the amplitude of

the MEP to a single unilateral test pulse with the MEP amplitude to a unilateral

magnetic test pulse which is preceded by a contralateral magnetic conditioning

pulse. When the test pulse is given 10 milliseconds (ms) after the conditioning

stimulus, a significant reduction in MEP size of the test response is observed

(Ferbert et al., 1992) . The fact that TCl is greatly reduced in patients with

callosal infarctions (Li, Lai, & Chen, 2012) and even absent in acallosal patients

(Meyer, R.i:iricht, & Woiciechowsky, 1998) suggests that the corpus callosum is the main mechanism underlying interhemispheric inhibition.

Using methods rhar interleave TMS with EEG (Komssi & Kahkonen, 2006), significantly higher levels of interhemispheric signal propagation from rhe right to the left side ofrhe brain were recently demonstrated in aggressive psychopathic

offenders as compared to healthy individuals (Hoppenbrouwers et a!., 20 14).

Aggressive psychopathic offenders also displayed increased local intra-cortical

inhibition of the right, bur nor rhe left motor cortex (Hoppenbrouwers er al.,

2013).Taken together, these ~lndings may suggest a less responsive right cerebral

hemisphere in aggres'>ive p'>ychoparhic otTenders rh.H results in reduced

comn1is-;ur.1l inhibition of the ,lpproach-rel.Hed motivational system of the left

cerebr,ll hemi'>phere (Hoppenbrouwers er al., 20 14). The latter ~lnding concurs

with recent results in which ,1 graph theoretical approach to study Jll.ltomical

connecti\·iry wa> med to demonstrate abnormalities in inrerregion,ll connectivity

parrerm of rhe right frontal cortex in psychopaths (Yang er a!., 20 12). The exact

mechanism driving rhe<,e e!Tecrs remains unclear .u rhi'> point; however. deficient

axonal pruning of commissural L'Xcirarory fibers during neural development

may at least in parr account for the lower level<, of rr.1nscallosal inhibition.

A compar.1blc commissural .!symmetric pattern has been observed in healthy

\·olunteers in which left-to-right mediated tramcallos.ll inhibition i'> po'>iti\·ely

corrcl.Hed to physical and verbal aggression. and relative dominant lefi:-to-right

m·er right-to-leti: transcallosal inhibition i'> predictive for -,electi\'L' .mentional

biase'> toward angry facial expressions (Hotinan & Schutter, 2009). These results

can be interpreted as a cerebral asymmetry that is caused by a dominant left­

sided approach system actively inhibiting rhe right-sided avoidance sy-;tem in

the CJse of more ,111gry aggressive response'>: or a dominant right-sided avoidance

system which actively down-regulates the lefi:--;ided approach system in the case

of lcs'> angry .1ggressive responses. Importantly, these ~lndings indic.ue that the

interrelation between rhe corpus callosum and aggression c.1n be demomtrated

in the normal population (Schutter & Harmon-Jones, 20 13).

I nrerestingly. alterations in callosal transmission may also provide a meclunism

for explaining the earlier rTMS findings on the processing of .mgry facial

expres-,iom. The inhibitory effects of rTMS locally down-regulate the excitatory

transcallosal output to rhe contralateral hemisphen:. caming a rransiem functional

decoupling and release of callosal inhibition rlut subsequenrly incre.1ses activity

in the opposite hemisphere. This view would be in line with rhe hemispheric

rivalry hypothesis of contralateral hyper.lctivity following unilateral lesions

(Kinsbourne, 1976). Alternatively, cross-reduction of cortical excitability following

inhibitory rTMS could be explained by axonal Ktivation of excitatory c.1llosal

~iber'> le.1ding ro inhibition of the contralateral hemi!>phere ,H higher stimulation

inremitic:-, (Wa.,sermann, Wedegaertner, Ziemann, George, & Chen, 199H). It has

also bc:en .,hown rhar alcohol intake causes transient reductions of functional

connniv,ural connectivity between the fronral hemi'>pheres (Hoppenbrouwers,

Hotman, & Schutter, 2009). Particularly, the callosal fibers running from the right hemisphere to the left seem to be most sensitive to the acute effects of moderate alcohol ingestion . This observation concurs with the idea of tilting hemispheric balance to a dominant relative left-sided cortical asymmetry caused by reduced right-sided innervations of inhibitory commissural fibers. The subsequent brain state, indicative of approach-related motivational tendencies and anger, could at least provide a partial biological account for the well-documented association

between alcohol and aggression . The proposed relation between abnormal

interhemispheric signal transfer and aggression is further underlined by a study that revealed a link between structural abnormalities of the corpus callosum and

sui cide behavior in the elderly community (Cyprien et al., 2011). In further

support o f the latter finding, another study found evidence for volumetric

reductions of the genu and isthmus regions of the corpus callosum in euthymic

patients suffering from bipolar disorder with a history of suicide attempts (Nery­

Fernandes et al., 2012). However, structural neuroimaging is not able to extract

information on the functional status of the corpus callosum and direction of

callosal signal transfer. However, based on the prior discussion, it can be

hypothesized that white-matter abnormalities associated with pathological forms

of aggression will be more pronounced in fibers running from the right to the

left hemisphere, arguably creating a motivational stance of diminished avoidance­

related and increased approach-related behavior. Taken together, the empirical

evidence from neuroimaging research and from recent non-invasive brain

stimulation studies suggests that the corpus callosum plays a significant role in

anger and aggressive behavior. However, even though the reviewed findings are

in line with the idea that the corpus callosum plays an important role in the

formation of cortical asynm1etries of mammals (e.g., Lent & Schmidt, 1993), they

do not necessarily provide a conclusive explanation of the cause of the inter­

cortical imbalance in relation to anger and aggression.

Although the corpus callosum constitutes the main structures responsible for

signal exchange between the cerebral hemispheres, the anterior commissure is

an additional forebrain bundle that provides a direct pathway for signal transfer

between the cerebral hemispheres. The an terior commissure is a mye linated

white-matter fiber tract that crosses th e midline of the brain anterior to the third

ventricle and connects parts of the temporal and orbitofrontal cortices as well

as the insular cortices and amygdala (Raybaud, 2010). From a neuroanatomical

perspective, th e anterior commissure probably plays a substantial role in

motivational processes on th e level of th e cerebral cortex . For example, the

anterior commissure can provide a link for the proposed role of the insular

cortices in understanding forebrain motivational asymmetries as asymmetric

representations of the autonomous nervous system (Craig, 2005). However,

except for one diffusion tensor imaging study showing that the anterior

commissure may be implicated in aggressive behavior in children with bipolar

disorder (Saxena et al., 2012), to our knowledge, no studies are available that

have looked into the role of the anterior commissure in anger and aggression. Finally, information exchange between the two ce rebral hemispheres can also occur indirectly via subcortica l polysy napti c pathways. In this context, the ce rebellar tracts may be of parti cular interest, as increas ing evidence suggests that the cerebellum is involved in affective processes (Schutter, 20 13).The cerebe llum rece ives input from th e ce rebral hemispheres via th e po ntine nuclei of th e brainstem, and projects back to the contralatera l ce rebral co rtex via the deep

ce rebellar nucle i (Middleton & Strick, 20()] ), layi ng an ana to mica l foundation

for info rmati o n exchange between the cerebral hemispheres. In addition, recent

findings suggest the ex istence of a cerebellar asym metry analogous to the cerebral

asymmetry (Wang, 13uckner, & Liu , 20 12).

Conclusion

N euroimag ing, psychophysio logical, and clinical po pulati o n studi es provide

conve rge nt evidence that social aggression is underpinned by ho rmo nally driven

imbalances within and between subcorti ca l and co rti cal leve ls of th e brain.

Neurobiologicall y, antagonistic ac ti ons between the H PG and H PA axes and

diametrically opposite behavio ral effec ts of the end products of these axes­

testOsterone and cortisol-are the fo undation of this model. Increased testOsterone

levels relative to cortisol levels predispose individuals toward approach motiva tio n ,

in which they automatically and non-consciously respond to potential threats

with dominance and aggression . Furthermo re, greater testosterone versus cortisol

leve ls redu ces subcortica l-cortical couplin g, redu cing the top- down control that

may help to inhibit further aggression. The fi·ontal co rtex also shows imbalances:

Left frontal corti cal activity is associated with approac h motivati o n and ange r,

whereas ri ght frontal cortical ac tivity is assoc iated with avo idance motiva ti o n

and anxiety (Harmon-Jones, 2003; van H onk e t a!. , 20 I 0). Additional lines of

inquiry suggest that directional differences in signal transmissio n between each

hemisph ere also figure cen trally in soc ial reac ti ve agg ress io n . R.ece nt

inte rhemispheric connectivity studies with TMS add an important aspec t to

what is currently known about the relati o ns between direc tional co rti ca l

asym m etri es, ange r, and aggression, and shed new light o n unrave ling the

biological mechanisms driving aggression . Distinct differences pertaining to the

direction of callosal signal transfer between the cortica l systems implica ted in

ap proach- and avo idance-related motivation are proposed to contribute to the

exp ressio n of ange r and aggression.

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13 CUlTURAl NEUROSCIENCE

Bridging Cultural and Biological Sciences

joan Y. Chiao and Katherine D. 8/izinsky

Introduction

The Cultural Neuroscience Framework

Culturcll neuro>cience is an inte rdiscipliiury tleld that imegrate'> theory clllll

methods from anthropo logy, cultural psychology, neurmcience , clnd genetin

to understand diversity in human behavior clcrms multiple time >cale'i (Chiao

& Ambcldy, ~()()7 ; Chiao, Cheon, Pornpattananclllgkul, MrclZek, & l3lizin,ky ,

~() 13: Cheon , Mrazek, Pornpattananangkul, l3lizimky. & Chiao. ~() 13; '>ee

Figure IJ.I ) . The idea ofswdyi ng human behavior cl'> an interactive by-product

of cultured ,1nd biological fac tors is not new; cliHhropologi'>tS have long examined

cultur.J! .md biologica l systems as a means of addre'>'>ing where hum.1n divn>iry

come'> tl·om and why. H owever, nor much theoretical or empirica l attention

has been p.1id previo usly to how culwral and biological -;ystems .,h,lpe thL·

hum.m brclin (Lende & Downey, 10 11). Theory and method in cultural

neuroscience are unique in rh ar this branch of neurmcience empha-,ize'> thL'

'>tudy of how cultura l, environmental, and biological f.1ctors can independently

.md inter.lctivcly shape neurobiological processes tlut predict human beh.wior

('>ee Figure 13.1) . Much progress in cu ltural p'>yc hology ha> occurred in

idemifying specific cu ltural val ues, practices, and belid~ rh ,n emerge due ro

environmuu.1l or ecological fac tors and subsequently .,h ,lpe behJ\'ior. Simi larly,

dL'C,lde'> of aLh-ances in human neuroscience and genL' tic-; ha\·e identified neural

.md genetic -,ysrems that forete ll human behavioral p.mcrm. H ence , much can

be ,Jchieved by integrating aspects of th ese disciplinL' '> in order ro gain a better

undcr.,tmdiiw of human diversity. . "'