1 Hz rTMS over the Right Prefrontal Cortex ReducesVigilant Attention to Unmasked but Not to MaskedFearful Faces

Jack van Honk, Dennis J.L.G. Schutter, Alfredo A.L. d’Alfonso, Roy P.C. Kessels,and Edward H.F. de Haan

Background: Recent repetitive transcranial magneticstimulation (rTMS) research in healthy subjects suggeststhat the emotions anger and anxiety are lateralized in theprefrontal cortex. Low-frequency rTMS over the rightprefrontal cortex (PFC) shifts the anterior asymmetry inbrain activation to the left hemisphere and reduces anxi-ety. The same rTMS technique results in enhanced anger-related emotional processing, observed as elevations inattention for angry faces. The current study used low-frequency rTMS over the right PFC and indexed selectiveattention to fearful faces, hypothesizing a reduction inattention for fearful faces, i.e., a reversal of the lattereffect.

Methods: In a placebo-controlled design, 1 Hz rTMS at130% of the individual motor threshold (MT) was appliedcontinuously over the right PFC of eight healthy subjectsfor 20 minutes. Effects on motivated attention were inves-tigated by means of an emotional Stroop task, indexingselective attention to masked and unmasked fearful faces.

Results: Vigilant attention for masked and unmaskedfearful faces was observed after placebo stimulation. Ashypothesized, rTMS reduced the vigilant emotional re-sponse to the fearful face, but only in the unmasked task.

Conclusions: These data provide further support for thelateralization of the emotions anger and anxiety in theprefrontal cortex. In addition, the absence of an effect formasked fearful faces suggests that changes in emotionalprocessing after a single session of rTMS predominantlyinvolve the cortical affective pathways. Biol Psychiatry2002;52:312–317 © 2002 Society of BiologicalPsychiatry

Key Words: rTMS, lateralization, fearful faces, motivatedattention, subcortical/cortical affective circuits

Introduction

In the human brain, emotion is regulated by a complexcompound of cortical and subcortical circuits (Damasio

et al 2000; Panksepp 1992). Gradually, neuroimagingstudies are beginning to unravel the underlying dynamicsof these affective processing pathways. In accordance withthe approach and withdrawal dimensions of the valencehypothesis (Davidson 1998), recent electroencephalo-graphic (EEG) studies have found evidence for the later-alization of the negative emotions anger and anxiety inthe prefrontal cortex (PFC). The left PFC is evidentlyinvolved in anger proneness and the expression of theapproach-related emotion anger (Coan et al 1999;Harmon-Jones and Allen 1998; Harmon-Jones andSigelman 2001), whereas the right PFC is involved infearful behavior and the expression of the withdrawal-related emotion fear (Coan et al 1999; Kalin et al 1998).

The cerebral cortex, however, is not necessarily impli-cated in the processing of anger and fear. Functionalneuroimaging studies have indicated that parallel to corti-cal routes, a primordial subcortical pathway to the amyg-dala might act as a neurobiological shortcut for fastactivation of the arousal system. When presented brieflyand backwardly masked, angry and fearful facial expres-sions are not consciously recognized, but neverthelessseem to be processed “unseen” by way of the thalamicnuclei (Morris et al 1999; Rauch et al 2000). Based on thisevidence, a simple model of human approach- and with-drawal-related affective information processing has beenconstructed (van Honk and de Haan 2001). In this model,the left and right prefrontal cortices are respectivelyinvolved in consciously controlled (and thus more sophis-ticated forms) of behavioral approach and withdrawal(Davidson 1998). Furthermore, a subcortical affectiveshortcut, the thalamic–amygdaloid pathway subserves themore biologically prepared emotional response, uncon-founded by conscious control (Ohman and Soares 1998;Ledoux 1996). Conscious control is mediated by orbito-frontal and medial structures of the prefrontal cortex

From the Helmholtz Research Institute, Affective Neuroscience Section, UtrechtUniversity, Utrecht, The Netherlands.

Address reprint requests to Jack van Honk, Ph.D., Helmholtz Research Institute,Utrecht University, Affective Neuroscience Section, Heidelberglaan 2, Utrecht3584 CS, The Netherlands.

Received September 4, 2001; revised January 8, 2002; accepted January 15, 2002.

© 2002 Society of Biological Psychiatry 0006-3223/02/$22.00PII S0006-3223(02)01346-X

(OMPFC). These OMPFC affective control and relaystations have strong afferent and efferent connections withthe dorsolateral prefrontal cortices and the amygdala(Fuster 1997). Because responses to masked and un-masked facial threat seem to provide insight in thedifference between subcortical and cortical human affec-tive information processing, facial threat might well beused to investigate a so-called attentional bias for threat,which characterizes emotional disorders (McNally 1995;Rauch et al 2000).

Recently, we set out to investigate the attentional biasfor angry and fearful faces. An emotional Stroop task wasused, comparing color-naming latencies of masked andunmasked neutral versus angry or fearful faces. It issuggested that the angry facial expression plays an impor-tant role in regulating social interactions. Vigilant atten-tion to the angry face would indicate an inclination todefend social status, i.e., face-to-face dominance (Mazurand Booth 1998; van Honk and de Haan 2001). Inagreement, subjects with high levels of the emotion angeror the hormone testosterone, both associated with inter-personal dominance, display vigilant attentional responsesto angry faces in the Stroop task (Van Honk et al 1999,2001). In contrast, the fearful face serves as a danger call,indicating that threat is perceived by a member of thesocial group, which might readily apply to the observer.Anxiety is accompanied by a preoccupation for danger.Therefore, anxious individuals should display vigilantattention to fearful faces. In concordance, the more vigi-lant attentional response to the fearful face is related tophysiologic and self-reported indices of anxiety (Hermanset al 1999). Notably, in the above line of research with theemotional Stroop task, the observed relations defy andsometimes even depend on backward masking (Hermanset al 1999; van Honk et al 1998, 2000a, 2001), suggestingthat the subcortical pathway is importantly involved inthese motivated aspects of attention (Morris et al 1999;Rauch et al 2000).

A technical innovation in neuroscience, repetitivetranscranial magnetic stimulation (rTMS), is capable ofestablishing functional brain–behavior relationships bymodulating brain activity in controlled designs (Pascual-Leone et al 1999). Moreover, recent studies suggestthat rTMS is capable of influencing mood and motivatedattention in ways that can be functionally linked to theapproach–withdrawal dimensions of behavior (i.e., angerand anxiety). Low-frequency rTMS (i.e., stimulation fre-quency �1 Hz) applied over the right dorsolateral PFCabove the motor threshold (MT) for thumb movement(i.e., suprathreshold intensity) reduces anxiety and shiftsthe anterior asymmetry in brain activation to the left(Schutter et al 2001). Furthermore, elevations in selectiveattention to unmasked angry faces were found after simi-

lar rTMS (d’Alfonso et al 2000), which are presumablyanger-related and possibly left-prefrontally driven emo-tional responses (Coan et al 1999; Harmon-Jones andAllen 1998; Harmon-Jones and Sigelman 2001; van Honket al 1999, 2001). Initially, this effect of low-frequencyrTMS is induced by a transient neural inhibition of thetargeted right PFC (Pascual-Leone et al 1998); however,distant effects in anatomically interconnected brain areashave also been observed using neuroimaging techniques(Speer et al 2000). For instance, low-frequency rTMS overthe left or right PFC at the suprathreshold intensitiesproduces contralateral excitation (Nahas et al 2001; Schut-ter et al 2001). This effect is possibly due to a reduction intranscallosal inhibition after the initial unilateral deactiva-tion of the targeted area (Pascual-Leone et al 1998;Schutter et al 2001).

In sum, owing to unilateral inhibition and/or contralat-eral excitation, suprathreshold low-frequency rTMS overthe right PFC seems to result in more left PFC–dominantprocessing, reductions in anxiety (Schutter et al 2001), andenhanced anger-related emotional processing (d’Alfonsoet al 2000). Taken together, these findings corroborateEEG evidence for the lateralization of the approach-related emotion anger and withdrawal-related emotionanxiety. Moreover, effects on motivated attention were notobserved in a lateralized, suprathreshold, low-frequencyrTMS study over the PFC when angry faces were pre-sented backwardly masked in the Stroop task (van Honkand d’Alfonso, unpublished data). This suggests thattransient changes in motivated attention induced by single-session rTMS predominantly take place on a cortical level.

The aim of the present rTMS study was to furtherinvestigate the anterior lateralization of the emotion anx-iety by using fearful faces in the Stroop task. In ad-dition, it was investigated whether rTMS would againinduce a selective effect when using a combined masked–unmasked Stroop paradigm (cf. d’Alfonso et al 2000;van Honk and d’Alfonso, unpublished data), because thiswould suggest that rTMS is capable of dissociating be-tween conscious and preconscious affective processing. Itwas hypothesized that suprathreshold, low-frequencyrTMS over the right PFC would reduce selective attentionto fearful faces in the unmasked task exclusively.

Methods and Materials

ParticipantsEight right-handed volunteers (four female) aged between 20and 26 years participated in this single-blind, crossover, coun-terbalanced, sham-controlled experiment. An informed consentwas obtained, and subjects with a history of neurologic orpsychiatric disorder were excluded. All participants were naiveof TMS and unaware of the aim of the study. The local ethicalcommittee of the Faculty of Social Sciences approved the study.

Prefrontal rTMS and Selective Attention to Fearful Faces 313BIOL PSYCHIATRY2002;52:312–317

ProcedureOn separate days, 1 Hz or placebo rTMS (Neopulse MagneticStimulator; Neotunus, Atlanta, GA) with an intensity of 130% ofthe MT for thumb movement was applied over the right PFC(position F4 according to the International 10–20 system) (seeFigure 1A). For placebo stimulation, the coil position was tilted90° (Schutter et al 2001). Thirty minutes after stimulation orplacebo, selective attention for masked and unmasked fearfulfaces was assessed using an emotional Stroop task comparingcolor-naming latencies for neutral and fearful faces. This 30-mindelay was used, because low-frequency rTMS research demon-strated delayed and extended effects in time on several indices ofemotional processing (d’Alfonso et al 1999; Schutter et al 2001;van Honk et al 2001).

Emotional Stroop TaskMasked and unmasked versions of an emotional Stroop task wereemployed to measure selective attention to fearful faces. This

task requires participants to name as quickly as possible the colorof pictures of fearful and neutral facial expressions (red, green,blue, and yellow) presented on a 160-Hz computer screen at adistance of 60 cm. The dependent measures in the emotionalStroop task are Attentional Bias scores (i.e., the mean individualcolor-naming latencies of fearful faces minus the individualmean color-naming latencies on neutral faces). Positive Atten-tional Bias scores, indicating slower color-naming responses toemotional compared to neutral stimuli, are interpreted as avigilant response, whereas the negative Attentional Bias score,indicating faster color naming responses to emotional comparedto neutral stimuli, is interpreted as an avoidant response. Thestimuli were taken from Ekman and Friesen’s Pictures of FacialAffect (Ekman and Friesen 1976). In the masked task, a fixationpoint was shown for 750 msec, followed by the target stimulus (aneutral or a fearful face) presented for 14 msec, before beingreplaced by a masking stimulus. Masking stimuli were randomlycut, reassembled, and re-photographed pictures of faces. Thepresentation of the mask was terminated after vocal responseinitiation (see Figure 1B). In the unmasked task, the fixationpoint was also shown for 750 msec and followed by the targetstimulus (a neutral or a fearful face), and target presentation wasterminated after vocal response initiation (see Figure 1C). In bothtasks, 40 neutral and 40 fearful faces were presented in randomorder with the restriction that the same color was never repeatedmore than twice consecutively. Stimulation and task conditionassignments were fully randomized.

Subliminal thresholds were controlled for by both a subjectiveand an objective awareness check (i.e., a forced-choice, emotion-al–neutral recognition check). Both checks were performed afterthe second session to ascertain that subjects remained unaware ofthe variable of interest in the Stroop task during the course of theexperiment. The subjective check was a simple interview askingsubjects whether they had recognized the emotional valence ofthe faces that were displayed before the masks. The objectivecheck was a two-alternative, forced-choice (2AFC) emotional–neutral recognition procedure. In this 2AFC, a random set of 30masked faces was shown to the subjects. In advance, subjectswere explicitly told that the set contained 15 neutral and 15fearful faces and were instructed to indicate (or guess), bypushing a button, whether the presented picture was a neutral oran emotional expression (see Kemp-Wheeler and Hill 1988, forthe rationale behind this instruction).

Results

There was no evidence of recognition of emotional va-lence during masked presentation, neither by subjectivenor by objective checks. Subjects’ performance in theobjective check did not differ from chance level (i.e., 15correct identifications per subject in a 2AFC recognitioncheck containing 30 stimuli). Of the total number ofidentifications (240), 121 were correct (50.4%). Individualupper limit was set at 19 correct scores. Nonparametrictests for deviation from the expected value (cut-point �15) were not significant (n � 8, p � 1). Thus, maskingwas successful.

Figure 1. (A) Position of stimulation, and sequence of stimuluspresentations in (B) masked and (C) unmasked condition.

314 J. van Honk et alBIOL PSYCHIATRY2002;52:312–317

Repeated multivariate analyses of variance were per-formed on the Attentional Bias scores, with STIM (stim-ulation: F4 vs. placebo) and EXPOSURE (unmasked vs.masked) as within-subject factors. Analyses showed asignificant main effect for both STIM [F(1,7) � 15.2; p �.01] and EXPOSURE [F(1,7) � 16.1; p � .01]. Therewas, however, also a significant multivariate STIM �EXPOSURE interaction [F(1,7) � 23.3; p � .005],indicating different effects of stimulation in masked andunmasked exposure conditions. Separate analyses of un-masked and masked data showed no effect of STIM in themasked task [F(1,7) � .3; ns], but a highly significanteffect in the unmasked task [F(1,7) � 19.7; p � .004]. Thepattern of results is shown in Figure 2.

Additionally, two-tailed paired t tests were performed tosee whether the Attentional Bias scores differed signifi-cantly from zero (i.e., indicating no bias). In the placebocondition there was a significant positive Attentional Biasfor the masked [t(7) � 3.5; p � .01] and the unmaskedtask[t(7) � 3.4; p � .015]. In the F4 stimulation conditionagain, a positive Attentional Bias was observed for themasked task [t(7) � 3.3; p � .015], but a negativeAttentional Bias was found for the unmasked task [t(7) ��3.1, p � .02].

Discussion

The present study investigated the effects of right PFCrTMS on attentional biases for masked and unmaskedfearful faces. Vigilant attention for fearful faces wasobserved both in the masked and in the unmasked expo-sure condition after placebo stimulation. As hypothesized,

rTMS significantly decreased vigilant attention for fearfulfaces in the unmasked but not in the masked task. Aspreviously suggested, this effect could have been inducedby a more left-sided dominance in prefrontal processing.As noted, combined rTMS neuroimaging studies did notonly show focal changes in activation of the targeted areas,but also demonstrated distant effects in anatomicallyinterconnected regions. Because these distant changes inactivation are supervening on the initial focal effect, theseare likely part of functionally connected (affective) net-works or neurons in the brain. Repetitive TMS neuroim-aging studies might in fact reveal these functionallyconnected networks of neurons and provide additionalinsight in the affective circuits of the human brain (cf. Foxet al 1997; Paus et al 1997).

Moreover, the present findings in the Stroop task canfunctionally be linked to left PFC–dominant processing asobserved by EEG (Coan et al 1999; Harmon-Jones andAllen 1998; Harmon-Jones and Sigelman 2001). Further-more, evidence from rTMS-EEG and rTMS-functionalmagnetic resonance imaging suggest that the presentrTMS parameters (when applied over the right PFC)induce a left-sided dominance (Nahas et al 2001; Schutteret al 2001). Finally, elevations in attention for angry faceswere demonstrated after suprathreshold low-frequencyrTMS over the right PFC (d’Alfonso et al 2000), incontrast to the current reductions in biased attention forfearful faces. Taken together, these findings seem tofurther support the involvement of the left PFC in thewithdrawal-related emotion anger, and the right PFC in theapproach-related emotion fear (Coan et al 1999; d’Alfonsoet al 2000; Harmon-Jones and Allen 1998; Harmon-Jonesand Sigelman 2001). In further support of this view,Figure 2 shows that biased attention for fearful faces wasreversed after rTMS from positive to negative scores in theunmasked task, which indicates that the processing of thefearful faces was strongly inhibited. Disregarding a dangersignal is a risky behavioral strategy and can most likely beobserved in low-anxiety, anger-prone individuals, with apresumably left PFC dominance (Coan et al 1999;d’Alfonso et al 2000; Fox 1991; Hermans et al 1999).

The current findings also show that the pattern ofresponding remains unchanged for the masked task afterrTMS. This is likely due to the inability of the rTMStechnique to directly modulate the emotional responsewhen the emotional stimulus remains unconscious. Asnoted previously, the left and the right PFCs are respec-tively involved in conscious control of behavioral ap-proach and withdrawal, whereas the thalamic–amygdaloidpathway subserves the rudimentary emotional response.The OMPFC contains the brain structures crucially in-volved in the modulation of emotion (Davidson et al 2000;van Honk et al 2000b), but requires conscious monitoring

Figure 2. Mean attentional bias scores and SEM in millisecondsfor the masked and unmasked tasks in placebo and transcranialmagnetic stimulation (TMS) condition. PFC, prefrontal cortex;rTMS, repetitive TMS.

Prefrontal rTMS and Selective Attention to Fearful Faces 315BIOL PSYCHIATRY2002;52:312–317

for acting out its emotional control (Reiman 1997). Inagreement, neuroimaging studies have shown no activa-tion in OMPFC regions when fearful and angry faces arepresented masked (Morris et al 1999; Rauch et al 2000).Because the OMPFC can only operate when gainingconscious access to emotional value (Davidson et al 2000;Reiman 1997), the modulation of the emotional responseto the masked fearful face arguably needs subcorticalmediation (van Honk et al 2000; van Honk and de Haan2001). It seems therefore justifiable to assume that thetransient suppression of motivated attention in the presentstudy was observed for the unmasked fearful face only,because the rTMS technique applied here induced func-tional changes in neural excitability of cortical affectivecircuits predominantly.

Finally, it may be noted that although rTMS did notinduce an effect in the masked task, the present studyfulfills all criteria for subliminal activation postulated byDixon (1981). There was positive evidence for subliminalactivation (1) in both the placebo and rTMS condition(i.e., vigilant attention to masked fearful faces). An objec-tive check of awareness was used, providing negativeevidence of awareness (2) in the masked task. The crucialqualitative different effect for masked and unmaskedstimuli (3) was also found, after real rTMS had beenapplied.

In conclusion, these data corroborate and extend thefindings of our earlier reports (d’Alfonso et al 2000;Schutter et al 2001) and provide further support for thedifferential involvement of the PFC in the emotions angerand fear (Coan et al 1999; Fox 1991; Harmon-Jones andAllen 1998; Harmon-Jones and Sigelman 2001). In addi-tion, the rTMS-induced effect for the unmasked but not themasked task concurs with data from neuroimaging studies(Morris et al 1999; Rauch et al 2000), providing furtherevidence for a possible dissociation between cortical andsubcortical affective circuits in the human brain.

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