Linking enhancing and impairing effects of emotion—the ...

OPINION ARTICLEpublished: 20 May 2013

doi: 10.3389/fnint.2013.00026

Linking enhancing and impairing effects of emotion—thecase of PTSDFlorin Dolcos1,2,3*

1 Psychology Department, University of Illinois at Urbana-Champaign, Champaign, IL, USA2 Neuroscience Program, University of Illinois at Urbana-Champaign, Champaign, IL, USA3 The Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Champaign, IL, USA*Correspondence: [email protected]

Edited by:

Lihong Wang, Duke University, USA

Reviewed by:

Lihong Wang, Duke University, USA

INTRODUCTIONAs illustrated by the present ResearchTopic, emotion that can either enhance orhinder various aspects of our cognitionand behavior. For instance, the emotionalcharge of an event can increase attention toand memory for that event (Dolcos et al.,2012), whereas task-irrelevant emotionalinformation may lead to increased distrac-tion away from goal-relevant tasks (Iordanet al., 2013; see also Dolcos et al., 2011).Interestingly, sometimes these opposingeffects of emotion co-occur. For example,hearing a gunshot may enhance memoryfor central aspects of what was happen-ing at the time, while impairing mem-ory for peripheral details (Christianson,1992). It is also possible that increaseddistraction from ongoing goals producedby task-irrelevant emotional stimuli maylead to better memory for the distract-ing information itself. The co-occurrenceof enhancing and impairing effects ofemotion is probably most evident in affec-tive disorders, where both of these oppos-ing effects are exacerbated. Specifically,uncontrolled recollection of and rumina-tion on distressing memories observed indepression and post-traumatic stress dis-order (PTSD) may also lead to impairedcognition due to enhanced emotionaldistraction. Here, we illustrate an examplebased on evidence from studies of PTSD,pointing to the importance of investigatingboth enhancing and impairing effects ofemotion, in elucidating the nature of alter-ations in the way emotion interacts withcognition in clinical conditions.

BACKGROUND: EMOTIONAL ANDCOGNITIVE PROCESSING IN PTSDChanges in emotional and cognitive pro-cessing are critical features in PTSDpatients, typically reflected in increased

emotional reactivity and recollection oftraumatic memories, along with impairedcognitive/executive control (Rauch et al.,2006; Shin and Liberzon, 2009; see also inthis issue Brown and Morey, 2012; Hayeset al., 2012). Of particular note is emerg-ing evidence concerning the neural cor-relates of alterations associated with theencoding of emotional memories (Hayeset al., 2011) and with the responsesto task-irrelevant emotional distraction(Morey et al., 2009). These changes arereflected in regions associated with func-tions that may be enhanced (episodicmemory) or impaired (working mem-ory) by emotion—i.e., the medial tempo-ral lobe (MTL) and dorsolateral prefrontalcortex (dlPFC), respectively. Here, weillustrate how understanding the changesassociated with the way traumatic mem-ories are formed and retrieved in PTSD(involving MTL areas) may clarify theirimpact on ongoing cognitive/executiveprocesses (reflected in changes of dlPFCactivity), when potential cues for trau-matic memories are presented as task irrel-evant distracters.

THE ENHANCING EFFECT OF EMOTIONStudies investigating the memory-enhancing effect of emotion in healthyparticipants point to the role of basicMTL mechanisms involving interac-tions between emotion-based regions(amygdala—AMY) and memory-relatedregions (hippocampus and associatedparahippocampal cortices—HC, PHC)in the formation and retrieval of emo-tional memories (Dolcos et al., 2012).Neurobiological models of PTSD (Laytonand Krikorian, 2002) propose that thedevelopment and maintenance of thedisorder is linked to altered activity inthe MTL during encoding of traumatic

memories. Hence, intrusive recollec-tion of traumatic memories observedin PTSD may be linked to dysfunctionof the basic MTL mechanism identi-fied in healthy participants as beingresponsible for the memory-enhancingeffect of emotion (Dolcos et al., 2004).Specifically, processing of cues related totraumatic events may trigger recollectionof traumatic memories, which due to dys-functional interactions between AMY andthe MTL memory system may engage aself-sustaining functional loop in whichemotion processing in AMY may enhancerecollection by increasing activity in HC;this, in turn, may intensify AMY activityas a result of re-experiencing the emotionsassociated with the recollected memories(Dolcos et al., 2005; McNally, 2006). Onthe other hand, there is also evidence sug-gesting a disconnect between the effectsobserved in AMY and their link to emo-tional or cognitive aspects of processing inPTSD patients. Specifically, while greaterAMY activation is identified in studies ofsymptom provocation (Rauch et al., 2000;Hendler et al., 2003; Shin et al., 2004, 2005;Williams et al., 2006), such an effect is notobserved in studies of cognitive process-ing (Shin et al., 2001; Clark et al., 2003;Bremner et al., 2004; Morey et al., 2008).

An important observation that hasemerged in the PTSD literature may recon-cile this apparent discrepancy. Specifically,there is evidence that memories for nega-tive events in PTSD patients may be non-specific, gist-based, rather than detailed,context-based (McNally et al., 1994; Kaspiet al., 1995; Harvey et al., 1998). Gist refersto familiarity-based retrieval of memo-ries for the general meaning of a situa-tion or event, rather than recollection ofspecific contextual details (Tulving, 1985).Given that gist-based memories are often

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INTEGRATIVE NEUROSCIENCE

Dolcos Emotion-Cognition Interactions in PTSD

inaccurate (Roediger and McDermott,1995; Wright and Loftus, 1998) and sus-ceptible to enhanced rate of false alarmsthat may diminish or cancel an actualenhancing impact of emotion on mem-ory (Dolcos et al., 2005), it may be thecase that the basic AMY-MTL mechanismstypically responsible for the memory-enhancing effect of emotion are in factattenuated in PTSD. Hence, this couldexplain the non-specific, gist-based, mem-ories observed in these patients. This ideais supported by recent findings from afMRI study using the subsequent memoryparadigm with emotional stimuli in PTSDpatients (Hayes et al., 2011), which showedreduced memory-related activity in theAMY-MTL system during memory encod-ing, and higher false alarm rates duringretrieval, compared to a trauma exposedcontrol (TEC) participants (Figure 1A).Moreover, the PTSD patients also lackedthe anterior posterior dissociation alongthe longitudinal axis of the MTL, withrespect to its involvement during suc-cessful encoding of emotional memories,which was initially identified in healthyparticipants (Dolcos et al., 2004), butsuch dissociation was preserved in theTEC group (Hayes et al., 2011). Together,these findings suggest a disorganizationof the MTL mechanisms involved in thememory-enhancing effect of emotion inPTSD, which leads to inefficient encodingof information for trauma-related stim-uli and subsequent non-specific gist-basedretrieval.

THE IMPAIRING EFFECT OF EMOTIONStudies investigating the neural correlatesof the impairing effect of task-irrelevantemotional distraction on cognitive per-formance identified distinct patternsof responses in emotion and cognitivecontrol brain regions (i.e., increased activ-ity in AMY and reduced activity in dlPFC,respectively), which are specific to emo-tional distraction (Dolcos et al., 2011).On the one hand, based on this evidence,increased emotional reactivity linked tochanges in the AMY function in PTSDmay lead to increased specific disruptionof dlPFC activity by emotional distrac-tion. On the other hand, there is evidencefor a non-specific heightened sensitivityto both threatening and non-threateningstimuli in PTSD (Grillon and Morgan,1999; Peri et al., 2000), which may explain

increased distractibility to trauma relatedand unrelated stimuli alike.

The fact that information unrelatedto the trauma may also be highly dis-tracting in PTSD patients is consistentwith the clinically observed symptom ofhypervigilance in these patients (AmericanPsychiatric Association, 2000), and withthe evidence for non-specific encoding oftrauma-related material discussed above(Hayes et al., 2011). Specifically, it is rea-sonable to expect that seemingly neu-tral stimuli that may remind of traumacould act as cues for non-specific retrievalof trauma-related information, which inturn may be as distracting as the trauma-related stimuli themselves. Evidence froma recent study of WM with trauma-related and non-related distraction is con-sistent with this idea (Morey et al., 2009).Using an adaptation of our WM taskwith emotional distraction (Dolcos andMcCarthy, 2006), the study by Moreyand colleagues investigated how trauma-related task-irrelevant emotional informa-tion modulates WM networks in PTSD.Similar to the study on memory encod-ing discussed above, recent post-9/11 warveterans were divided into a PTSD groupand a TEC group. Functional MRI resultsshowed that the PTSD group had greatertrauma-specific activation than the controlgroup in main emotion processing brainregions, including the AMY and ventro-lateral PFC (vlPFC), as well as in brainregions susceptible to emotion modula-tion (e.g., fusiform gyrus—FG). However,the PTSD group also showed greaternon-specific disruption of activity tocombat-related and neutral task-irrelevantdistracters in brain regions that subservethe ability to maintain focus on goal-relevant information, including the dlPFC.This suggests a more generalized dlPFCdisruption in the PTSD group than inthe control group, which showed disrup-tion specific to the trauma-related distrac-tion. The undifferentiated dlPFC responseto combat and non-combat distracters inPTSD is consistent with the hypervigilancehypothesis that may explain enhancedresponse to and distracting effect of neu-tral stimuli (Figure 1C). This neural-levelfinding was complemented by the behav-ioral results, which showed lower overallworking memory performance for task-irrelevant distracters scenes in the PTSDgroup, in the absence of a differential

impact between combat-related and neu-tral distracters.

THE LINK BETWEEN ENHANCING ANDIMPAIRING EFFECTS OF EMOTIONOverall, the evidence from separate lines ofinvestigations discussed above, regardingthe neural changes in PTSD linked to dys-functions in the recollection of traumaticevents and the response to emotional dis-traction, converge toward the idea thatnon-specific response to emotional andneutral distraction may reflect retrievaldistortions linked to inefficient initialencoding of trauma-related information.Namely, it is possible that the non-specific disruption of the dlPFC activityby trauma-related and neutral distractionis linked to the retrieval of the traumaticmemories triggered by non-specific cues,which may also contribute to the per-petuation of the state of hyperarousalobserved in these patients (Figure 1D).Moreover, it is also possible that the sourceof these effects may be linked to elevatedarousal during the initial exposure to trau-matic events. Consistent with this idea, inaddition to showing non-specific activ-ity to subsequently remembered itemsin AMY and MTL memory system inPTSD, the study by Hayes and colleaguesdiscussed above (Hayes et al., 2011)also identified a negative co-variationof memory-related hippocampal activ-ity for trauma-related items with scores ofhyperarousal symptoms, as measured withthe Clinician-Administered PTSD Scale(Figure 1B). In other words, participantswho had greater hyperarousal scores alsohad reduced memory-related activityduring the encoding of trauma-relatedpictures. This finding is consistent withevidence for an inverted U-shaped func-tion in the hippocampus as a functionof stress (Nadel and Jacobs, 1998) andprovides a possible explanation for thenon-specific effects observed in the tasksassessing emotional memory for trauma-related cues and their undifferentiatedimpact on goal-relevant processing whenpresented as task-irrelevant distraction.Consistent with the role of the initialarousal in these effects, PTSD patientsalso showed relatively greater activity forforgotten items, which may be linkedto AMY hyperactivity leading to laterforgetting of those items (Hayes et al.,2011).

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Dolcos Emotion-Cognition Interactions in PTSD

FIGURE 1 | (A–B) Memory-Related Changes in the Medial Temporal LobeActivity in PTSD. Reduced memory-related activity (Dm) in AMY fortrauma-related pictures, in the PTSD group (A); a similar effect was alsoobserved in the HC (not shown). Reduced Dm for trauma-related picturesin the anterior HC linked to increased symptoms of arousal (B). Dm,Difference due to Memory effect (brain activity for Remembered minusForgotten items); PTSD, post-traumatic stress disorder; TEC,Trauma-Exposed Control group; AMY, Amygdala; HC, Hippocampus;PHC, Parahippocampal Cortex; Ant, Anterior; Post, Posterior. Error barsrepresent the standard error of means. Adapted from Hayes et al. (2011),with permission. (C) Evidence for Non-specific Response in dlPFC to

Trauma-Related and Neutral Distracters in PTSD. Comparison of meanpercentage signal change in dlPFC during the active maintenance periodof a working memory task in the PTSD and Trauma-Exposed Control(TEC) groups point to a generalized dlPFC disruption of activation forsalient task-irrelevant distracter scenes in the PTSD group, which showedan undifferentiated response in the dlPFC to combat and neutraldistracters. The TEC group showed disruption in the same area, butspecific to combat-related distraction. dlPFC, dorsolateral prefrontal cortex.Adapted from Morey et al. (2009), with permission. (D) Diagramillustrating a possible link between the impact of emotion on long-termmemory and working memory in PTSD.

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Dolcos Emotion-Cognition Interactions in PTSD

CONCLUSIONIn summary, available evidence frominvestigations of PTSD patients points togeneral and specific emotional and cogni-tive disturbances that are linked to alter-ations in the neural circuitry underlyingemotion-cognition interactions. This evi-dence suggests that reduction of AMYand HC signals for trauma-related cuesmay underlie non-specific encoding ofgist-based representations instead of spe-cific and detailed contextual details of thetrauma-related memories. This, in turn,may be linked to symptoms of hyper-vigilance and non-specific responses totrauma-related distraction, which con-tributes to the maintenance of a hyper-arousal state (Figure 1D). This evidencealso highlights the importance of inves-tigating both the enhancing and theimpairing effects of emotion, in under-standing the changes associated withaffective disorders, where both effectsare intensified. Collectively, these findingspoint to the importance of investigatingboth of these opposing effects of emotionwithin the same clinical group, to comple-ment similar approaches in healthy par-ticipant concomitantly investigating theenhancing and impairing effects of emo-tion on cognitive processes (Shafer andDolcos, 2012; Dolcos et al., 2013).

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Received: 10 February 2013; accepted: 01 April 2013;published online: 20 May 2013.Citation: Dolcos F (2013) Linking enhancing andimpairing effects of emotion—the case of PTSD. Front.Integr. Neurosci. 7:26. doi: 10.3389/fnint.2013.00026Copyright © 2013 Dolcos. This is anopen-access article distributed under the terms ofthe Creative Commons Attribution License, whichpermits use, distribution and reproduction in otherforums, provided the original authors and source arecredited and subject to any copyright notices concerningany third-party graphics etc.

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