Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system

Steuwe C, Daniels JK, Frewen PA, Densmore M, Pannasch S, Beblo T, Reiss J, Lanius RA (2014)
Social Cognitive and Affective Neuroscience 9(1): 88-97.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Steuwe, Carolin; Daniels, Judith K.; Frewen, Paul A.; Densmore, Maria; Pannasch, Sebastian; Beblo, ThomasUniBi; Reiss, Jeffrey; Lanius, Ruth A.
Abstract / Bemerkung
In healthy individuals, direct eye contact initially leads to activation of a fast subcortical pathway, which then modulates a cortical route eliciting social cognitive processes. The aim of this study was to gain insight into the neurobiological effects of direct eye-to-eye contact using a virtual reality paradigm in individuals with posttraumatic stress disorder (PTSD) related to prolonged childhood abuse. We examined 16 healthy comparison subjects and 16 patients with a primary diagnosis of PTSD using a virtual reality functional magnetic resonance imaging paradigm involving direct vs averted gaze (happy, sad, neutral) as developed by Schrammel et al. in 2009. Irrespective of the displayed emotion, controls exhibited an increased blood oxygenation level-dependent response during direct vs averted gaze within the dorsomedial prefrontal cortex, left temporoparietal junction and right temporal pole. Under the same conditions, individuals with PTSD showed increased activation within the superior colliculus (SC)/periaqueductal gray (PAG) and locus coeruleus. Our findings suggest that healthy controls react to the exposure of direct gaze with an activation of a cortical route that enhances evaluative 'top-down' processes underlying social interactions. In individuals with PTSD, however, direct gaze leads to sustained activation of a subcortical route of eye-contact processing, an innate alarm system involving the SC and the underlying circuits of the PAG.
social cognition; fMRI; childhood abuse; dorsomedial prefrontal; superior colliculus; cortex; PTSD
Social Cognitive and Affective Neuroscience
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Steuwe C, Daniels JK, Frewen PA, et al. Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience. 2014;9(1):88-97.
Steuwe, C., Daniels, J. K., Frewen, P. A., Densmore, M., Pannasch, S., Beblo, T., Reiss, J., et al. (2014). Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience, 9(1), 88-97. doi:10.1093/scan/nss105
Steuwe, C., Daniels, J. K., Frewen, P. A., Densmore, M., Pannasch, S., Beblo, T., Reiss, J., and Lanius, R. A. (2014). Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience 9, 88-97.
Steuwe, C., et al., 2014. Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience, 9(1), p 88-97.
C. Steuwe, et al., “Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system”, Social Cognitive and Affective Neuroscience, vol. 9, 2014, pp. 88-97.
Steuwe, C., Daniels, J.K., Frewen, P.A., Densmore, M., Pannasch, S., Beblo, T., Reiss, J., Lanius, R.A.: Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Social Cognitive and Affective Neuroscience. 9, 88-97 (2014).
Steuwe, Carolin, Daniels, Judith K., Frewen, Paul A., Densmore, Maria, Pannasch, Sebastian, Beblo, Thomas, Reiss, Jeffrey, and Lanius, Ruth A. “Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system”. Social Cognitive and Affective Neuroscience 9.1 (2014): 88-97.

21 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Role of social cognition in post-traumatic stress disorder: A review and meta-analysis.
Stevens JS, Jovanovic T., Genes Brain Behav 18(1), 2019
PMID: 30221467
Superior colliculus resting state networks in post-traumatic stress disorder and its dissociative subtype.
Olivé I, Densmore M, Harricharan S, Théberge J, McKinnon MC, Lanius R., Hum Brain Mapp 39(1), 2018
PMID: 29134717
The neural correlates of Childhood Trauma Questionnaire scores in adults: A meta-analysis and review of functional magnetic resonance imaging studies.
Heany SJ, Groenewold NA, Uhlmann A, Dalvie S, Stein DJ, Brooks SJ., Dev Psychopathol 30(4), 2018
PMID: 29224580
Threat Bias and Emotion Recognition in Victims of IPV.
Clauss K, Clements C., J Interpers Violence (), 2018
PMID: 29598751
Resting-state pulvinar-posterior parietal decoupling in PTSD and its dissociative subtype.
Terpou BA, Densmore M, Théberge J, Frewen P, McKinnon MC, Lanius RA., Hum Brain Mapp 39(11), 2018
PMID: 30091811
Neurobiology of comorbid post-traumatic stress disorder and alcohol-use disorder.
Gilpin NW, Weiner JL., Genes Brain Behav 16(1), 2017
PMID: 27749004
Intranasal oxytocin increases neural responses to social reward in post-traumatic stress disorder.
Nawijn L, van Zuiden M, Koch SB, Frijling JL, Veltman DJ, Olff M., Soc Cogn Affect Neurosci 12(2), 2017
PMID: 27614769
Accessible Neurobehavioral Anger-Related Markers for Vulnerability to Post-Traumatic Stress Symptoms in a Population of Male Soldiers.
Lin T, Gilam G, Raz G, Or-Borichev A, Bar-Haim Y, Fruchter E, Hendler T., Front Behav Neurosci 11(), 2017
PMID: 28326027
The role of automatic defensive responses in the development of posttraumatic stress symptoms in police recruits: protocol of a prospective study.
Koch SBJ, Klumpers F, Zhang W, Hashemi MM, Kaldewaij R, van Ast VA, Smit AS, Roelofs K., Eur J Psychotraumatol 8(1), 2017
PMID: 29321826
Amygdala selectively modulates defensive responses evoked from the superior colliculus in non-human primates.
Forcelli PA, DesJardin JT, West EA, Holmes AL, Elorette C, Wellman LL, Malkova L., Soc Cogn Affect Neurosci 11(12), 2016
PMID: 27510499
Aberrant Functional Connectivity of the Amygdala Complexes in PTSD during Conscious and Subconscious Processing of Trauma-Related Stimuli.
Rabellino D, Densmore M, Frewen PA, Théberge J, McKinnon MC, Lanius RA., PLoS One 11(9), 2016
PMID: 27631496
fMRI functional connectivity of the periaqueductal gray in PTSD and its dissociative subtype.
Harricharan S, Rabellino D, Frewen PA, Densmore M, Théberge J, McKinnon MC, Schore AN, Lanius RA., Brain Behav 6(12), 2016
PMID: 28032002
Moral reasoning in women with posttraumatic stress disorder related to childhood abuse.
Nazarov A, Walaszczyk V, Frewen P, Oremus C, Lanius R, McKinnon MC., Eur J Psychotraumatol 7(), 2016
PMID: 27837580
Violence-related PTSD and neural activation when seeing emotionally charged male-female interactions.
Moser DA, Aue T, Suardi F, Kutlikova H, Cordero MI, Rossignol AS, Favez N, Rusconi Serpa S, Schechter DS., Soc Cogn Affect Neurosci 10(5), 2015
PMID: 25062841
Performance monitoring and behavioral adaptation during task switching: an fMRI study.
von der Gablentz J, Tempelmann C, Münte TF, Heldmann M., Neuroscience 285(), 2015
PMID: 25446349
Reward functioning in PTSD: a systematic review exploring the mechanisms underlying anhedonia.
Nawijn L, van Zuiden M, Frijling JL, Koch SB, Veltman DJ, Olff M., Neurosci Biobehav Rev 51(), 2015
PMID: 25639225
Oxytocin's role in anxiety: a critical appraisal.
MacDonald K, Feifel D., Brain Res 1580(), 2014
PMID: 24468203

65 References

Daten bereitgestellt von Europe PubMed Central.

Amygdala responses to averted vs direct gaze fear vary as a function of presentation speed
Adams RB, Franklin RG, Kveraga K., 2011

Role of the locus coeruleus in emotional activation.
Aston-Jones G, Rajkowski J, Kubiak P, Valentino RJ, Shipley MT., Prog. Brain Res. 107(), 1996
PMID: 8782532
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

Baron-Cohen S., 1995
Development and validation of a brief screening version of the Childhood Trauma Questionnaire.
Bernstein DP, Stein JA, Newcomb MD, Walker E, Pogge D, Ahluvalia T, Stokes J, Handelsman L, Medrano M, Desmond D, Zule W., Child Abuse Negl 27(2), 2003
PMID: 12615092
Ascending visceral regulation of cortical affective information processing.
Berntson GG, Sarter M, Cacioppo JT., Eur. J. Neurosci. 18(8), 2003
PMID: 14622171
The development of a Clinician-Administered PTSD Scale.
Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM., J Trauma Stress 8(1), 1995
PMID: 7712061

Prior electrical stimulation of dorsal periaqueductal grey matter or deep layers of the superior colliculus sensitizes rats to anxiety-like behaviors in the elevated T-maze test.
de Almeida LP, Ramos PL, Pandossio JE, Landeira-Fernandez J, Zangrossi H Jr, Nogueira RL., Behav. Brain Res. 170(2), 2006
PMID: 16569447
Emotion in the brain: of low roads, high roads and roads less travelled
de B, van J, Tamietto M., 2011
Processing social aspects of human gaze: a combined fMRI-DTI study.
Ethofer T, Gschwind M, Vuilleumier P., Neuroimage 55(1), 2010
PMID: 21095230
Processing angry and neutral faces in post-traumatic stress disorder: an event-related potentials study
Felmingham KL, Bryant RA, Gordon E., 2003

First MB, Spitzer RL, Gibbon M, Williams JBW., 1996
Assessment of anhedonia in psychological trauma: development of the Hedonic Deficit and Interference Scale
Frewen PA, Dean AD, Lanius RA., 2012
Neuroimaging social emotional processing in women: fMRI study of script-driven imagery.
Frewen PA, Dozois DJ, Neufeld RW, Densmore M, Stevens TK, Lanius RA., Soc Cogn Affect Neurosci 6(3), 2010
PMID: 20525743
Brain activation to facial expressions in youth with PTSD symptoms.
Garrett AS, Carrion V, Kletter H, Karchemskiy A, Weems CF, Reiss A., Depress Anxiety 29(5), 2012
PMID: 22553009
Neurophysiological networks integrating human emotions
Halgren E, Marinkovic K., 1995
Looking at you or looking elsewhere: the influence of head orientation on the signal value of emotional facial expressions
Hess U, Adams RB, Kleck RE., 2007
Subcortical face processing
Johnson MH., 2005
Arousal systems.
Jones BE., Front. Biosci. 8(), 2003
PMID: 12700104
Eye tracking and visual attention to threating stimuli in veterans of the Iraq war.
Kimble MO, Fleming K, Bandy C, Kim J, Zambetti A., J Anxiety Disord 24(3), 2010
PMID: 20138463
Functional grouping and cortical–subcortical interactions in emotion: a meta-analysis of neuroimaging studies
Kober H, Feldman L, Joseph J., 2008

Krill WE, McKinnon M., 2010
Duration matters: dissociating neural correlates of detection and evaluation of social gaze.
Kuzmanovic B, Georgescu AL, Eickhoff SB, Shah NJ, Bente G, Fink GR, Vogeley K., Neuroimage 46(4), 2009
PMID: 19328236
Pretense and representation: the origins of “theory of mind”
Leslie AM., 1987
A direct brainstem-amygdala-cortical 'alarm' system for subliminal signals of fear.
Liddell BJ, Brown KJ, Kemp AH, Barton MJ, Das P, Peduto A, Gordon E, Williams LM., Neuroimage 24(1), 2005
PMID: 15588615
A temporal dissociation of subliminal versus supraliminal fear perception: an event-related potential study.
Liddell BJ, Williams LM, Rathjen J, Shevrin H, Gordon E., J Cogn Neurosci 16(3), 2004
PMID: 15072682
Type I and Type II error concerns in fMRI research: re-balancing the scale.
Lieberman MD, Cunningham WA., Soc Cogn Affect Neurosci 4(4), 2009
PMID: 20035017
Panic disorder—a malfunction of multiple transmitter control systems within the midbrain periaqueductal gray matter?
Lovick TA., 2000
The effects of self-involvement on attention, arousal, and facial expression during social interaction with virtual others: a psychophysiological study.
Mojzisch A, Schilbach L, Helmert JR, Pannasch S, Velichkovsky BM, Vogeley K., Soc Neurosci 1(3-4), 2006
PMID: 18633787
The cognitive basis of a biological disorder: autism
Morton J, Frith U, Leslie AM., 1991

Panksepp J., 1998
Emotion processing: from a ‘low road’ to’many roads’ of evaluating biological significance
Pessoa L, Adolphs R., 2010
Abnormal modulation of amygdala activity in schizophrenia in response to direct- and averted-gaze threat-related facial expressions.
Pinkham AE, Loughead J, Ruparel K, Overton E, Gur RE, Gur RC., Am J Psychiatry 168(3), 2010
PMID: 21159729
Does it make a difference if I have an eye contact with you or with your picture? An ERP study.
Ponkanen LM, Alhoniemi A, Leppanen JM, Hietanen JK., Soc Cogn Affect Neurosci 6(4), 2010
PMID: 20650942
Does the chimpanzee have a theory of mind?
Premack D, Woodruff G., 1978
Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study.
Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, Orr SP, Pitman RK., Biol. Psychiatry 47(9), 2000
PMID: 10812035
Overlapping and non-overlapping brain regions for theory of mind and self reflection in individual subjects.
Saxe R, Moran JM, Scholz J, Gabrieli J., Soc Cogn Affect Neurosci 1(3), 2006
PMID: 18985110
The thing that should not be: predictive coding and the uncanny valley in perceiving human and humanoid robot actions.
Saygin AP, Chaminade T, Ishiguro H, Driver J, Frith C., Soc Cogn Affect Neurosci 7(4), 2011
PMID: 21515639
Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry.
Schilbach L, Wilms M, Eickhoff SB, Romanzetti S, Tepest R, Bente G, Shah NJ, Fink GR, Vogeley K., J Cogn Neurosci 22(12), 2010
PMID: 19929761
Being with virtual others: Neural correlates of social interaction.
Schilbach L, Wohlschlaeger AM, Kraemer NC, Newen A, Shah NJ, Fink GR, Vogeley K., Neuropsychologia 44(5), 2005
PMID: 16171833
Virtual friend or threat? The effects of facial expression and gaze interaction on psychophysiological responses and emotional experience.
Schrammel F, Pannasch S, Graupner ST, Mojzisch A, Velichkovsky BM., Psychophysiology 46(5), 2009
PMID: 19470127
The eye contact effect: mechanisms and development.
Senju A, Johnson MH., Trends Cogn. Sci. (Regul. Ed.) 13(3), 2009
PMID: 19217822
A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder.
Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, Macklin ML, Lasko NB, Cavanagh SR, Krangel TS, Orr SP, Pitman RK, Whalen PJ, Rauch SL., Arch. Gen. Psychiatry 62(3), 2005
PMID: 15753240
Thresholds of electrically induced defence reaction of the rat: short- and long-term adaptation mechanisms.
Sudre EC, de Barros MR, Sudre GN, Schenberg LC., Behav. Brain Res. 58(1-2), 1993
PMID: 8136042
Shared intentionality.
Tomasello M, Carpenter M., Dev Sci 10(1), 2007
PMID: 17181709
Social cognition and the brain: a meta-analysis.
Van Overwalle F., Hum Brain Mapp 30(3), 2009
PMID: 18381770
Mind reading: neural mechanisms of theory of mind and self-perspective.
Vogeley K, Bussfeld P, Newen A, Herrmann S, Happe F, Falkai P, Maier W, Shah NJ, Fink GR, Zilles K., Neuroimage 14(1 Pt 1), 2001
PMID: 11525326
Essential functions of the human self model are implemented in the prefrontal cortex.
Vogeley K, Kurthen M, Falkai P, Maier W., Conscious Cogn 8(3), 1999
PMID: 10487788
The centrencephalon and thalamocortical integration: neglected contributions of periaqueductal gray
Watt DF., 2000

Whiten A., 1991

Wilkinson M., 2010
Trauma modulates amygdala and medial prefrontal responses to consciously attended fear.
Williams LM, Kemp AH, Felmingham K, Barton M, Olivieri G, Peduto A, Gordon E, Bryant RA., Neuroimage 29(2), 2005
PMID: 16216534
The human amygdala and the emotional evaluation of sensory stimuli.
Zald DH., Brain Res. Brain Res. Rev. 41(1), 2003
PMID: 12505650


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