12 - social emotive neuroscience lab · cyberostracism: effects ofbeing ignored over the internet....
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222 Moieni & Eisenberger
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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. . "'