Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-25T11:37:32.478Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural response to angry and disgusted facial expressions in bulimia nervosa

Published online by Cambridge University Press:  04 May 2011

F. Ashworth ,
A. Pringle ,
R. Norbury ,
C. J. Harmer ,
P. J. Cowen  and
M. J. Cooper
F. Ashworth
Affiliation:
Oxford Doctoral Course in Clinical Psychology, University of Oxford, UK
A. Pringle
Affiliation:
Psychopharmacology and Emotion Research Laboratory (PERL), Department of Psychiatry, University of Oxford, UK
R. Norbury
Affiliation:
Psychopharmacology Research Unit (PPRU), Department of Psychiatry, University of Oxford, UK
C. J. Harmer
Affiliation:
Psychopharmacology and Emotion Research Laboratory (PERL), Department of Psychiatry, University of Oxford, UK
P. J. Cowen
Affiliation:
Psychopharmacology Research Unit (PPRU), Department of Psychiatry, University of Oxford, UK
M. J. Cooper*
Affiliation:
Oxford Doctoral Course in Clinical Psychology, University of Oxford, UK
*
*Address for correspondence: Dr M. J. Cooper, Isis Education Centre, University of Oxford, Warneford Hospital, Oxford OX3 7JX, UK. (Email: myra.cooper@hmc.ox.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Processing emotional facial expressions is of interest in eating disorders (EDs) as impairments in recognizing and understanding social cues might underlie the interpersonal difficulties experienced by these patients. Disgust and anger are of particular theoretical and clinical interest. The current study investigated the neural response to facial expressions of anger and disgust in bulimia nervosa (BN).

Method

Participants were 12 medication-free women with BN in an acute episode (mean age 24 years), and 16 age-, gender- and IQ-matched healthy volunteers (HVs). Functional magnetic resonance imaging (fMRI) was used to examine neural responses to angry and disgusted facial expressions.

Results

Compared with HVs, patients with BN had a decreased neural response in the precuneus to facial expressions of both anger and disgust and a decreased neural response to angry facial expressions in the right amygdala.

Conclusions

The neural response to emotional facial expressions in BN differs from that found in HVs. The precuneus response may be consistent with the application of mentalization theory to EDs, and the amygdala response with relevant ED theory. The findings are preliminary, but novel, and require replication in a larger sample.

Keywords

Angerbulimia nervosadisgustfacial expressionsneuroimaging
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 11 , November 2011 , pp. 2375 - 2384
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, AK, Christoff, K, Panitz, D, De Rosa, E, Gabrieli, JDE (2003). Neural correlates of the automatic processing of threat facial signals. Journal of Neuroscience 23, 5627–5633.Google Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text revision. American Psychiatric Association: Washington, DC.Google Scholar
Beck, AT, Freeman, A, and Associates (1990). Cognitive Therapy of Personality Disorders. Guilford: New York.Google Scholar
Blair, RJB, Morris, SJ, Frith, CD, Perrett, DI, Dolan, RJ (1999). Dissociable neural response to facial expressions of sadness and anger. Brain 122, 883–893.Google Scholar
Calder, AJ, Keane, J, Manes, F, Antoun, N, Young, AW (2000). Impaired recognition and experience of disgust following brain injury. Nature Neuroscience 3, 1077–1078.Google Scholar
Campbell, DW, Sareen, J, Paulus, MP, Goldin, PR, Stein, MB, Reiss, JP (2007). Time varying amygdala response to emotional faces in generalised social phobia. Biological Psychiatry 62, 455–463.Google Scholar
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583.Google Scholar
Cooper, MJ, Todd, G, Wells, A (2009). Treating Bulimia Nervosa and Binge Eating: An Integrated Metacognitive and Cognitive Therapy Manual. Taylor & Francis: London.Google Scholar
Corstorphine, E, Mountford, V, Tomlinson, S, Glenn Waller, G, Meyer, C (2007). Distress tolerance in the eating disorders. Eating Behaviors 8, 91–97.Google Scholar
Darwin, C (1965). The Expression of Emotions in Man and Animals. University of Chicago Press: Chicago, IL.CrossRefGoogle Scholar
Davey, GCL, Buckland, G, Tantow, B, Dallos, R (1998). Disgust and eating disorders. European Eating Disorders Review 6, 201–211.Google Scholar
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K (2002). Depression: perspectives from affective neuroscience. Annual Review of Psychology 53, 545–574.CrossRefGoogle ScholarPubMed
Etkin, A, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476–1488.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (1996). Structured Clinical Interview for DSM-IV – Clinician Version (SCID-CV) (User's Guide). American Psychiatric Press: Washington, DC.Google Scholar
Fonagy, P, Gergely, G, Jurist, EL, Target, M (2002). Affect Regulation, Mentalization and the Development of the Self. Other Press: New York.Google Scholar
Fossati, P, Hevenor, SJ, Lepage, M, Graham, SJ, Grady, C, Keightley, ML, Craik, F, Mayberg, H (2004). Distributed self in episodic memory: neural correlates of successful retrieval of self-encoded positive and negative personality traits. NeuroImage 22, 1596–1604.CrossRefGoogle ScholarPubMed
Fox, JRE, Harrison, A (2008). The relation of anger to disgust: the potential role of coupled emotions within eating pathology. Journal of Clinical Psychology and Psychotherapy 15, 86–95.CrossRefGoogle ScholarPubMed
Freeman, D, Garety, PA, Phillips, ML (2000). An examination of hypervigilance for external threat in individuals with generalized anxiety disorder and individuals with persecutory delusions using visual scan paths. Quarterly Journal of Experimental Psychology Section A: Human Experimental Psychology 53, 549–567.Google Scholar
Friston, KJ, Jezzard, P, Turner, R (1994). The analysis of functional MRI time-series. Human Brain Mapping 1, 153–171.Google Scholar
Fusar-Poli, P, Placentino, A, Carletti, F, Landi, P, Allen, P, Surguladze, S, Benedetti, F, Abbamonte, M, Gasparotti, R, Barale, F, Perez, J, McGuire, P, Politi, P (2009). Functional atlas of emotional face processing: a voxel based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience 34, 418–432.Google Scholar
Garner, DM, Olmsted, MP, Bohr, Y, Garfinkel, PE (1982). The Eating Attitudes Test: psychometric features and clinical correlates. Psychological Medicine 12, 871–878.CrossRefGoogle ScholarPubMed
Green, MJ, Phillips, ML (2004). Social threat perception and the evolution of paranoia. Neuroscience and Biobehavioural Reviews 28, 333–342.Google Scholar
Green, MJ, Williams, LM, Davidson, D (2003). Visual scanpaths to threat related faces in deluded schizophrenia. Psychiatry Research 119, 271–285.Google Scholar
Hariri, AR, Bookheimer, SY, Mazziotta, JC (2000). Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 11, 43–48.Google Scholar
Harmer, CJ, Perrett, DI, Cowen, PJ, Goodwin, GM (2001). Administration of the beta-adrenoceptor blocker propranolol impairs the processing of facial expressions of sadness. Psychopharmacology (Berlin) 154, 383–389.Google Scholar
Hinrichsen, H, Wright, F, Waller, G, Meyer, C (2003). Social anxiety and coping strategies in the eating disorders. Eating Behaviors 4, 117–126.CrossRefGoogle ScholarPubMed
Jabbi, M, Swart, M, Keysers, C (2007). Empathy for positive and negative emotions in the gustatory cortex. NeuroImage 34, 1744–1753.Google Scholar
Jänsch, C, Harmer, CJ, Cooper, MJ (2009). Emotional processing in women with anorexia nervosa and healthy volunteers. Eating Behaviours 10, 184–191.Google Scholar
Jenkinson, M, Bannister, P, Brady, M, Smith, S (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825–841.Google Scholar
Jones, L, Harmer, CJ, Cowen, PJ, Cooper, MJ (2008). Emotional face processing in women with high and low levels of eating disorder related symptoms. Eating Behaviors 9, 389–397.Google Scholar
Joos, AAB, Cabrillac, E, Hartmann, A, Wirsching, M, Zeeck, A (2009). Emotional perception in eating disorder. International Journal of Eating Disorders 42, 318–325.Google Scholar
Kessler, H, Schwarze, M, Filipic, S, Traue, HC, von Wietersheim, J (2006). Alexithymia and facial emotion recognition in patients with eating disorders. International Journal of Eating Disorders 39, 245–251.Google Scholar
Knight, DC, Nguyen, HT, Bandettini, PA (2005). The role of the human amygdala in the production of conditioned fear responses. Neuroimage 26, 1193–1200.CrossRefGoogle ScholarPubMed
Krolak-Salmon, P, Henaff, MA, Isnard, J, Tallon-Baudry, C, Guenot, M, Vighetto, A, Bertrand, O, Mauguière, F (2003). An attention modulated response to disgust in human ventral anterior insula. Annals of Neurology 53, 446–453.Google Scholar
Kucharska-Pietura, K, Nikolaou, V, Masiak, M, Treasure, J (2003). The recognition of emotion in the faces and voice of anorexia nervosa. International Journal of Eating Disorders 35, 42–47.CrossRefGoogle Scholar
Kühnpast, N, Pollatos, O, Schandry, R (2009). Emotional face processing in bulimia nervosa: an ERP and source localization study. Clinical Neurophysiology 120, e67.Google Scholar
Lebrecht, S, Badre, D (2008). Emotional regulation, or how I learned to stop worrying and love the nucleus accumbens. Neuron 59, 841–843.Google Scholar
Leppänen, JM (2006). Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinion in Psychiatry 19, 34–39.CrossRefGoogle ScholarPubMed
Luck, A, Waller, G, Meyer, C, Ussher, M, Lacey, H (2005). The role of schema processes in the eating disorders. Cognitive Therapy and Research 29, 717–723.Google Scholar
Matsumoto, J, Eckman, P (1988). Japanese and Caucasian Facial Expressions of Emotion (JACFEE) and Neutral Faces (JACNeuF). Human Interaction Laboratory: San Francisco, CA.Google Scholar
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry 156, 675–682.Google Scholar
Mendlewicz, L, Linkowski, P, Bazelmans, C, Philippot, P (2005). Decoding emotional facial expressions in depressed and anorexic patients. Journal of Affective Disorders 89, 195–199.CrossRefGoogle ScholarPubMed
Morris, JS, Öhman, A, Dolan, RJ (1999). A subcortical pathway to the right amygdala mediating ‘unseen’ fear. Proceedings of the National Academy of Sciences USA 96, 1680–1685.Google Scholar
Nakamura, K, Kawashima, R, Ito, K, Sugiura, M, Kato, T, Nakamura, A, Hatano, K, Nagumo, S, Kubota, K, Fukuda, H, Kojima, S (1999). Activation of the right inferior frontal cortex during assessment of facial emotion. Journal of Neurophysiology 82, 1610–1614.Google Scholar
Nomura, M, Ohira, H, Haneda, K, Iidaka, T, Sadato, N, Okada, T, Yonekura, Y (2004). Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. NeuroImage 21, 352–363.Google Scholar
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JDE (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Science 14, 1215–1229.Google ScholarPubMed
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242–249.Google Scholar
Ofek, E, Pratt, H (2005). Neurophysiological correlates of subjective significance. Clinical Neurophysiology 116, 2354–2362.Google Scholar
Pallister, E, Waller, G (2008). Anxiety in the eating disorders: understanding the overlap. Clinical Psychology Review 28, 366–386.Google Scholar
Pegna, AJ, Khateb, A, Lazeyras, F, Seghier, ML (2004). Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neuroscience 8, 24–25.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.Google Scholar
Phillips, ML, Medford, N, Young, AW, Williams, L, Williams, SCR, Bullmore, ET, Gray, JA, Brammer, MJ (2001). Time courses of left and right amygdalar responses to fearful facial stimulation. Human Brain Mapping 12, 193–202.Google Scholar
Phillips, ML, Young, AW, Senior, C, Brammer, M, Andrew, C, Calder, AJ, Bullmore, ET, Perrett, DI, Rowland, D, Williams, SCR, Gray, JA, David, AS (1997). A specific neural substrate for perceiving facial expressions of disgust. Nature 389, 495–498.Google Scholar
Pollatos, O, Herbert, BM, Schandry, R, Gramann, K (2008). Impaired central processing of emotional faces in anorexia nervosa. Psychosomatic Medicine 70, 701–708.Google Scholar
Rothman, KJ (1990). No adjustments are needed for multiple comparisons. Epidemiology 1, 43–46.Google Scholar
Schienle, A, Vaitl, D, Schäfer, A (2010). Regional grey matter volume abnormalities in bulimia nervosa and binge-eating disorder. NeuroImage 50, 639–643.Google Scholar
Skråderud, F (2007 a). Eating one's words, Part 1: ‘Concretised metaphors’ and reflective function in anorexia nervosa – an interview study. European Eating Disorders Review 15, 163–174.Google Scholar
Skråderud, F (2007 b). Eating one's words, Part 111. Mentalisation-based psychotherapy for anorexia nervosa – an outline for a treatment and training manual. European Eating Disorders Review 15, 323–339.CrossRefGoogle Scholar
Smith, SM, Jenkinson, M, Woolrich, MW, Beckman, CF, Behrens, TE, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Nizzy, RK, Saounders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MRI image analysis and implementation as FSL. NeuroImage 23, S208–S219.Google Scholar
Surguladze, SA, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SC, Phillips, ML (2005). A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biological Psychiatry 57, 201–209.Google Scholar
Uher, R, Murphy, T, Brammer, MJ, Dalgleish, T, Phillips, ML, Ng, VW, Andrew, CM, Williams, SCR, Campbell, IC, Treasure, J (2004). Medial prefrontal cortex activity associated with symptom provocation in eating disorders. American Journal of Psychiatry 161, 1238–1246.Google Scholar
von dem Hagen, EAH, Beaver, JD, Ewbank, MP, Keane, J, Passamonti, L, Lawrence, AD, Calder, AJ (2009). Leaving a bad taste in your mouth but not in my insula. Social Cognitive and Affective Neuroscience 4, 379–386.Google Scholar
Waller, G, Babbs, M, Milligan, R, Meyer, C, Ohanian, V, Leung, N (2003). Anger and core beliefs in the eating disorders. International Journal of Eating Disorders 34, 118–124.Google Scholar
Waller, G, Cordery, H, Corstorophine, E, Hinrichsen, H, Lawson, R, Mountford, V, Russell, K (2007). Cognitive Behavioural Therapy for Eating Disorders: A Comprehensive Treatment Guide. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Wicker, B, Keysers, C, Plailly, J, Royet, JP, Gallese, V, Rizzolatti, G (2003). Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40, 655–664.Google Scholar
Woolrich, MW, Behrens, TE, Beckmann, CF, Jenkinson, M, Smith, SM (2004). Multilevel linear modelling for fMRI group analysis using Bayesian inference. NeuroImage 21, 1732–1747.Google Scholar
Woolrich, MW, Ripley, BD, Brady, M, Smith, SM (2001). Temporal autocorrection in univariate linear modelling of fMRI data. NeuroImage 14, 1370–1386.CrossRefGoogle Scholar
Young, JE (1994). Cognitive Therapy for Personality Disorders: A Schema-Focused Approach, 2nd edn. Professional Resource Press: Sarasota, FL.Google Scholar
Zigmond, AS, Snaith, RP (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica 67, 361–370.Google Scholar
Zonnevylle-Bender, MJS, van Goozen, SHM, Cohen-Kettenis, PT, van Elburg, A, van Engeland, H (2002). Do adolescent anorexia nervosa patients have deficits in emotional functioning? European Child and Adolescent Psychiatry 11, 38–42.Google Scholar