Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons

Eden AS, Dehmelt V, Bischoff M, Zwitserlood P, Kugel H, Keuper K, Zwanzger P, Dobel C (2015)
Frontiers in Psychology 6: 1226.

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Persons suffering from anxiety disorders display facilitated processing of arousing and negative stimuli, such as negative words. This memory bias is reflected in better recall and increased amygdala activity in response to such stimuli. However, individual learning histories were not considered in most studies, a concern that we meet here. Thirty-four female persons (half with high-, half with low trait anxiety) participated in a criterion-based associative word-learning paradigm, in which neutral pseudowords were paired with aversive or neutral pictures, which should lead to a valence change for the negatively paired pseudowords. After learning, pseudowords were tested with fMRI to investigate differential brain activation of the amygdala evoked by the newly acquired valence. Explicit and implicit memory was assessed directly after training and in three follow-ups at 4-day intervals. The behavioral results demonstrate that associative word-learning leads to an explicit (but no implicit) memory bias for negatively linked pseudowords, relative to neutral ones, which confirms earlier studies. Bilateral amygdala activation underlines the behavioral effect: Higher trait anxiety is correlated with stronger amygdala activation for negatively linked pseudowords than for neutrally linked ones. Most interestingly, this effect is also present for negatively paired pseudowords that participants could not remember well. Moreover, neutrally paired pseudowords evoked higher amygdala reactivity than completely novel ones in highly anxious persons, which can be taken as evidence for generalization. These findings demonstrate that few word-learning trials generate a memory bias for emotional stimuli, indexed both behaviorally and neurophysiologically. Importantly, the typical memory bias for emotional stimuli and the generalization to neutral ones is larger in high anxious persons.
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Frontiers in Psychology
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1226
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Eden AS, Dehmelt V, Bischoff M, et al. Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons. Frontiers in Psychology. 2015;6: 1226.
Eden, A. S., Dehmelt, V., Bischoff, M., Zwitserlood, P., Kugel, H., Keuper, K., Zwanzger, P., et al. (2015). Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons. Frontiers in Psychology, 6, 1226. doi:10.3389/fpsyg.2015.01226
Eden, A. S., Dehmelt, V., Bischoff, M., Zwitserlood, P., Kugel, H., Keuper, K., Zwanzger, P., and Dobel, C. (2015). Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons. Frontiers in Psychology 6:1226.
Eden, A.S., et al., 2015. Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons. Frontiers in Psychology, 6: 1226.
A.S. Eden, et al., “Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons”, Frontiers in Psychology, vol. 6, 2015, : 1226.
Eden, A.S., Dehmelt, V., Bischoff, M., Zwitserlood, P., Kugel, H., Keuper, K., Zwanzger, P., Dobel, C.: Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons. Frontiers in Psychology. 6, : 1226 (2015).
Eden, Annuschka S., Dehmelt, Vera, Bischoff, Matthias, Zwitserlood, Pienie, Kugel, Harald, Keuper, Kati, Zwanzger, Peter, and Dobel, Christian. “Brief learning induces a memory bias for arousing-negative words: an fMRI study in high and low trait anxious persons”. Frontiers in Psychology 6 (2015): 1226.
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The effect of anxiety on emotional recognition: evidence from an ERP study.
Yu Q, Zhuang Q, Wang B, Liu X, Zhao G, Zhang M., Sci Rep 8(1), 2018
PMID: 30385790
Emerging Directions in Emotional Episodic Memory.
Dolcos F, Katsumi Y, Weymar M, Moore M, Tsukiura T, Dolcos S., Front Psychol 8(), 2017
PMID: 29255432

112 References

Daten bereitgestellt von Europe PubMed Central.

Comparison of EEG propagation speeds under emotional stimuli on smartphone between the different anxiety states.
Asakawa T, Muramatsu A, Hayashi T, Urata T, Taya M, Mizuno-Matsumoto Y., Front Hum Neurosci 8(), 2014
PMID: 25540618

Baayen R., Piepenbrock R., Gulikers L.., 1995
Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study.
Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, van IJzendoorn MH., Psychol Bull 133(1), 2007
PMID: 17201568
An inventory for measuring depression.
BECK AT, WARD CH, MENDELSON M, MOCK J, ERBAUGH J., Arch. Gen. Psychiatry 4(), 1961
PMID: 13688369
Sleep and cortisol interact to support memory consolidation.
Bennion KA, Mickley Steinmetz KR, Kensinger EA, Payne JD., Cereb. Cortex 25(3), 2013
PMID: 24072888
Common and distinct neural correlates of facial emotion processing in social anxiety disorder and Williams syndrome: A systematic review and voxel-based meta-analysis of functional resonance imaging studies.
Binelli C, Subira S, Batalla A, Muniz A, Sugranyes G, Crippa JA, Farre M, Perez-Jurado L, Martin-Santos R., Neuropsychologia 64(), 2014
PMID: 25194208
fMRI reveals amygdala activation to human faces in social phobics.
Birbaumer N, Grodd W, Diedrich O, Klose U, Erb M, Lotze M, Schneider F, Weiss U, Flor H., Neuroreport 9(6), 1998
PMID: 9601698
Mood and memory.
Bower GH., Am Psychol 36(2), 1981
PMID: 7224324
Self-serving biases in the attribution process: a re-examination of the fact or fiction question.
Bradley G.., 1978
Remembering pictures: pleasure and arousal in memory.
Bradley MM, Greenwald MK, Petry MC, Lang PJ., J Exp Psychol Learn Mem Cogn 18(2), 1992
PMID: 1532823
Measuring emotion: the Self-Assessment Manikin and the Semantic Differential.
Bradley MM, Lang PJ., J Behav Ther Exp Psychiatry 25(1), 1994
PMID: 7962581
Five days versus a lifetime: intense associative vocabulary training generates lexically integrated words.
Breitenstein C, Zwitserlood P, de Vries MH, Feldhues C, Knecht S, Dobel C., Restor. Neurol. Neurosci. 25(5-6), 2007
PMID: 18334767
Examining attentional biases underlying trait anxiety in younger and older adults.
Burgess MM, Cabeleira CM, Cabrera I, Bucks RS, MacLeod C., Cogn Emot 28(1), 2013
PMID: 23768080
Ego-threat interpretative bias in test anxiety: On-line inferences.
Calvo M., Eysenck M., Estevez A.., 1994
Self-threat magnifies the self-serving bias: a meta-analytic integration.
Campbell W., Sedikides C.., 1999
Words as anchors: known words facilitate statistical learning.
Cunillera T, Camara E, Laine M, Rodriguez-Fornells A., Exp Psychol 57(2), 2010
PMID: 20178930
Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMRI study.
Dannlowski U, Ohrmann P, Bauer J, Kugel H, Arolt V, Heindel W, Kersting A, Baune BT, Suslow T., J Psychiatry Neurosci 32(6), 2007
PMID: 18043766
Amygdala reactivity predicts automatic negative evaluations for facial emotions.
Dannlowski U, Ohrmann P, Bauer J, Kugel H, Arolt V, Heindel W, Suslow T., Psychiatry Res 154(1), 2006
PMID: 17182226
The amygdala: vigilance and emotion.
Davis M, Whalen PJ., Mol. Psychiatry 6(1), 2001
PMID: 11244481
Non-native phonemes in adult word learning: evidence from the N400m.
Dobel C, Lagemann L, Zwitserlood P., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 364(1536), 2009
PMID: 19933141
New names for known things: on the association of novel word forms with existing semantic information.
Dobel C, Junghofer M, Breitenstein C, Klauke B, Knecht S, Pantev C, Zwitserlood P., J Cogn Neurosci 22(6), 2010
PMID: 19583468
Revise the revised? New dimensions of the neuroanatomical hypothesis of panic disorder.
Dresler T, Guhn A, Tupak SV, Ehlis AC, Herrmann MJ, Fallgatter AJ, Deckert J, Domschke K., J Neural Transm (Vienna) 120(1), 2012
PMID: 22692647
Emotion regulation and trait anxiety are predicted by the microstructure of fibers between amygdala and prefrontal cortex.
Eden AS, Schreiber J, Anwander A, Keuper K, Laeger I, Zwanzger P, Zwitserlood P, Kugel H, Dobel C., J. Neurosci. 35(15), 2015
PMID: 25878275
All in its proper time: monitoring the emergence of a memory bias for novel, arousing-negative words in individuals with high and low trait anxiety.
Eden AS, Zwitserlood P, Keuper K, Junghofer M, Laeger I, Zwanzger P, Dobel C., PLoS ONE 9(6), 2014
PMID: 24887093
A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder.
Evans KC, Wright CI, Wedig MM, Gold AL, Pollack MH, Rauch SL., Depress Anxiety 25(6), 2008
PMID: 17595018
Implicit memory bias, explicit memory bias, and anxiety.
Eysenck M., Byrne A.., 1994
Anxiety and cognitive performance: attentional control theory.
Eysenck MW, Derakshan N, Santos R, Calvo MG., Emotion 7(2), 2007
PMID: 17516812
Emotion and the processing of symbolic gestures: an event-related brain potential study.
Flaisch T, Hacker F, Renner B, Schupp HT., Soc Cogn Affect Neurosci 6(1), 2010
PMID: 20212003
Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold.
Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC., Magn Reson Med 33(5), 1995
PMID: 7596267
Human thalamic and amygdala modulation in emotional scene perception.
Frank DW, Sabatinelli D., Brain Res. 1587(), 2014
PMID: 25173075
Explicit memory bias for threat words in generalized anxiety disorder.
Friedman B., Thayer J., Borkovec T.., 2000
Double dissociation between memory systems underlying explicit and implicit memory in the human brain.
Gabrieli J., Fleischman D., Keane M., Reminger S.., 1995
A meta-analytic review of mood-congruent implicit memory in depressed mood.
Gaddy MA, Ingram RE., Clin Psychol Rev 34(5), 2014
PMID: 24980699
An fMRI study of emotional face processing in adolescent major depression.
Hall LM, Klimes-Dougan B, Hunt RH, Thomas KM, Houri A, Noack E, Mueller BA, Lim KO, Cullen KR., J Affect Disord 168(), 2014
PMID: 25036008
A rating scale for depression.
HAMILTON M., J. Neurol. Neurosurg. Psychiatry 23(), 1960
PMID: 14399272
Event related potentials to emotional adjectives during reading.
Herbert C, Junghofer M, Kissler J., Psychophysiology 45(3), 2008
PMID: 18221445
Vivid memories of emotional events: the accuracy of remembered minutiae.
Heuer F, Reisberg D., Mem Cognit 18(5), 1990
PMID: 2233262
Brain activation to briefly presented emotional words: effects of stimulus awareness.
Hoffmann M, Mothes-Lasch M, Miltner WH, Straube T., Hum Brain Mapp 36(2), 2014
PMID: 25324170
Linguistic threat activates the human amygdala.
Isenberg N, Silbersweig D, Engelien A, Emmerich S, Malavade K, Beattie B, Leon AC, Stern E., Proc. Natl. Acad. Sci. U.S.A. 96(18), 1999
PMID: 10468630
Repetition suppression of faces is modulated by emotion.
Ishai A, Pessoa L, Bikle PC, Ungerleider LG., Proc. Natl. Acad. Sci. U.S.A. 101(26), 2004
PMID: 15210952
Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression.
Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ., J. Neurosci. 27(33), 2007
PMID: 17699669
Fleeting images: a new look at early emotion discrimination.
Junghofer M, Bradley MM, Elbert TR, Lang PJ., Psychophysiology 38(2), 2001
PMID: 11347862
Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication.
Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE., Arch. Gen. Psychiatry 62(6), 2005
PMID: 15939837
How 'love' and 'hate' differ from 'sleep': using combined electro/magnetoencephalographic data to reveal the sources of early cortical responses to emotional words.
Keuper K, Zwanzger P, Nordt M, Eden A, Laeger I, Zwitserlood P, Kissler J, Junghofer M, Dobel C., Hum Brain Mapp 35(3), 2012
PMID: 23281129
Early prefrontal brain responses to the Hedonic quality of emotional words--a simultaneous EEG and MEG study.
Keuper K, Zwitserlood P, Rehbein MA, Eden AS, Laeger I, Junghofer M, Zwanzger P, Dobel C., PLoS ONE 8(8), 2013
PMID: 23940642
Buzzwords: early cortical responses to emotional words during reading.
Kissler J, Herbert C, Peyk P, Junghofer M., Psychol Sci 18(6), 2007
PMID: 17576257
Emotion and attention in visual word processing: an ERP study.
Kissler J, Herbert C, Winkler I, Junghofer M., Biol Psychol 80(1), 2008
PMID: 18439739
Components of attentional bias to threat in high trait anxiety: Facilitated engagement, impaired disengagement, and attentional avoidance.
Koster EH, Crombez G, Verschuere B, Van Damme S, Wiersema JR., Behav Res Ther 44(12), 2006
PMID: 16480943
The amygdala encodes level of perceived fear but not emotional ambiguity in visual scenes.
Kryklywy JH, Nantes SG, Mitchell DG., Behav. Brain Res. 252(), 2013
PMID: 23769997
Amygdala responsiveness to emotional words is modulated by subclinical anxiety and depression.
Laeger I, Dobel C, Dannlowski U, Kugel H, Grotegerd D, Kissler J, Keuper K, Eden A, Zwitserlood P, Zwanzger P., Behav. Brain Res. 233(2), 2012
PMID: 22659393
Have we met before? Neural correlates of emotional learning in women with social phobia.
Laeger I, Keuper K, Heitmann C, Kugel H, Dobel C, Eden A, Arolt V, Zwitserlood P, Dannlowski U, Zwanzger P., J Psychiatry Neurosci 39(3), 2014
PMID: 24758944
Of 'disgrace' and 'pain'--corticolimbic interaction patterns for disorder-relevant and emotional words in social phobia.
Laeger I, Dobel C, Radenz B, Kugel H, Keuper K, Eden A, Arolt V, Zwitserlood P, Dannlowski U, Zwanzger P., PLoS ONE 9(11), 2014
PMID: 25396729

Lang P., Bradley M., Cuthbert B.., 1999
The involvement of the left motor cortex in learning of a novel action word lexicon.
Liuzzi G, Freundlieb N, Ridder V, Hoppe J, Heise K, Zimerman M, Dobel C, Enriquez-Geppert S, Gerloff C, Zwitserlood P, Hummel FC., Curr. Biol. 20(19), 2010
PMID: 20888226
An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets.
Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH., Neuroimage 19(3), 2003
PMID: 12880848
Mood-congruent recall of affectively toned stimuli: a meta-analytic review.
Matt G., Vázquez C., Campbell W.., 1992
Implicit and explicit memory for threat words in high– and low-anxiety-sensitive participants.
McCabe R.., 1999
Early cortical processing of natural and artificial emotional faces differs between lower and higher socially anxious persons.
Muhlberger A, Wieser MJ, Herrmann MJ, Weyers P, Troger C, Pauli P., J Neural Transm (Vienna) 116(6), 2008
PMID: 18784899
Attentional requirements of learning: evidence from performance measures.
Nissen M., Bullemer P.., 1987
Selective memory effects in nonclinical panickers.
Norton G., Schaefer E., Cox B., Dorward J., Wozney K.., 1988
The assessment and analysis of handedness: the Edinburgh inventory.
Oldfield RC., Neuropsychologia 9(1), 1971
PMID: 5146491
Sleep’s role in the consolidation of emotional episodic memories.
Payne J., Kensinger E.., 2010
Sleep leads to changes in the emotional memory trace: evidence from FMRI.
Payne JD, Kensinger EA., J Cogn Neurosci 23(6), 2010
PMID: 20521852
Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia.
Phan KL, Fitzgerald DA, Nathan PJ, Tancer ME., Biol. Psychiatry 59(5), 2005
PMID: 16256956
Words in the brain’s language.
Pulvermüller F.., 1999
Common and specific brain responses to scenic emotional stimuli.
Radua J, Sarro S, Vigo T, Alonso-Lana S, Bonnin CM, Ortiz-Gil J, Canales-Rodriguez EJ, Maristany T, Vieta E, Mckenna PJ, Salvador R, Pomarol-Clotet E., Brain Struct Funct 219(4), 2013
PMID: 23700105
Fear generalization in the primate amygdala.
Resnik J, Paz R., Nat. Neurosci. 18(2), 2014
PMID: 25531573
Dissociation of the neural correlates of implicit and explicit memory.
Rugg MD, Mark RE, Walla P, Schloerscheidt AM, Birch CS, Allan K., Nature 392(6676), 1998
PMID: 9560154
On the status of implicit memory bias in anxiety.
Russo R, Fox E, Bowles RJ., Cogn Emot 13(4), 1999
PMID: 18273397
Mood-congruent free recall bias in anxious individuals is not a consequence of response bias.
Russo R, Whittuck D, Roberson D, Dutton K, Georgiou G, Fox E., Memory 14(4), 2006
PMID: 16766443
Constraints on statistical language learning.
Saffran J.., 2002
Statistical learning by 8-month-old infants.
Saffran JR, Aslin RN, Newport EL., Science 274(5294), 1996
PMID: 8943209
The selective processing of briefly presented affective pictures: an ERP analysis.
Schupp HT, Junghofer M, Weike AI, Hamm AO., Psychophysiology 41(3), 2004
PMID: 15102130
The facilitated processing of threatening faces: an ERP analysis.
Schupp HT, Ohman A, Junghofer M, Weike AI, Stockburger J, Hamm AO., Emotion 4(2), 2004
PMID: 15222855
Early emotion word processing: evidence from event-related potentials.
Scott GG, O'Donnell PJ, Leuthold H, Sereno SC., Biol Psychol 80(1), 2008
PMID: 18440691
The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10.
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC., J Clin Psychiatry 59 Suppl 20(), 1998
PMID: 9881538
Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study.
Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA., Biol. Psychiatry 50(9), 2001
PMID: 11704071
The neurocircuitry of fear, stress, and anxiety disorders.
Shin LM, Liberzon I., Neuropsychopharmacology 35(1), 2010
PMID: 19625997

Spielberger C., Gorsuch R., Lushene R., Vagg P., Jacobs G.., 1983
Verbal and motor memory in the amnestic syndrome.
Starr A, Phillips L., Neuropsychologia 8(1), 1970
PMID: 4330935
Rapid and highly resolving: affective evaluation of olfactorily conditioned faces.
Steinberg C, Dobel C, Schupp HT, Kissler J, Elling L, Pantev C, Junghofer M., J Cogn Neurosci 24(1), 2011
PMID: 21671742
Brain mechanisms for detecting perceptual, semantic, and emotional deviance.
Strange BA, Henson RN, Friston KJ, Dolan RJ., Neuroimage 12(4), 2000
PMID: 10988036
Brain activation during direct and indirect processing of positive and negative words.
Straube T, Sauer A, Miltner WH., Behav. Brain Res. 222(1), 2011
PMID: 21440008
Neural correlates of affective priming effects based on masked facial emotion: an fMRI study.
Suslow T, Kugel H, Ohrmann P, Stuhrmann A, Grotegerd D, Redlich R, Bauer J, Dannlowski U., Psychiatry Res 211(3), 2012
PMID: 23131525
Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: an fMRI study.
Tabert MH, Borod JC, Tang CY, Lange G, Wei TC, Johnson R, Nusbaum AO, Buchsbaum MS., Neuropsychologia 39(6), 2001
PMID: 11257281
Effect of negative emotional pictures on associative memory for peripheral information.
Touryan SR, Marian DE, Shimamura AP., Memory 15(2), 2007
PMID: 17534109
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M., Neuroimage 15(1), 2002
PMID: 11771995
Trait anxiety, working memory capacity, and the effectiveness of memory suppression.
Waldhauser GT, Johansson M, Backstrom M, Mecklinger A., Scand J Psychol 52(1), 2010
PMID: 21054419
Mechanisms of visual threat detection in specific phobia.
Weierich MR, Treat TA., Cogn Emot 29(6), 2014
PMID: 25251896
The emotional Stroop task and psychopathology.
Williams JM, Mathews A, MacLeod C., Psychol Bull 120(1), 1996
PMID: 8711015

Williams J., Watts F., MacLeod C., Mathews A.., 1988

Williams J., Watts F., MacLeod C., Mathews A.., 1997
Neural basis of emotional decision making in trait anxiety.
Xu P, Gu R, Broster LS, Wu R, Van Dam NT, Jiang Y, Fan J, Luo YJ., J. Neurosci. 33(47), 2013
PMID: 24259585
Encoding details: positive emotion leads to memory broadening.
Yegiyan NS, Yonelinas AP., Cogn Emot 25(7), 2011
PMID: 21756077
Attribution of success and failure revisited, or: the motivational bias is alive and well in attribution theory.
Zuckerman M.., 1979

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