Hostname: page-component-669899f699-vbsjw Total loading time: 0 Render date: 2025-04-26T10:33:42.823Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurophysiological correlates of disorder-related autobiographical memory in anorexia nervosa

Published online by Cambridge University Press:  18 June 2021

Valentin Terhoeven ,
Christoph Nikendei ,
Sandra Faschingbauer ,
Julia Huber ,
Kymberly D. Young ,
Martin Bendszus ,
Wolfgang Herzog ,
Hans-Christoph Friederich  and
Joe J. Simon
Valentin Terhoeven
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Christoph Nikendei
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Sandra Faschingbauer
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Julia Huber
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Kymberly D. Young
Affiliation:
The Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Martin Bendszus
Affiliation:
Department of Neuroradiology, University Hospital of Heidelberg, Heidelberg, Germany
Wolfgang Herzog
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Hans-Christoph Friederich
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
Joe J. Simon*
Affiliation:
Department of General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Heidelberg, Germany
*
Author for correspondence: Joe J. Simon, E-mail: joe.simon@med.uni-heidelberg.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Anorexia nervosa (AN) is characterized by an overgeneralization of food/body-related autobiographical memories (AM). This is regarded as an emotion regulation strategy with adverse long-term effects implicated in disorder maintenance and treatment resistance. Therefore, we aimed to examine neural correlates of food/body-related AM-recall in AN.

Methods

Twenty-nine female patients with AN and 30 medication-free age-sex-matched normal-weight healthy controls (HC) underwent functional magnetic resonance imaging while recalling AMs in response to food/body-related and neutral cue words. To control for general knowledge retrieval, participants engaged in a semantic generation and riser detection task.

Results

In comparison to HC, patients with AN generated fewer and less specific AMs in response to food/body-related words, but not for neutral cue words. Group comparisons revealed reduced activation in regions associated with self-referential processing and memory retrieval (precuneus and angular gyrus) during the retrieval of specific food/body-related AM in patients with AN. Brain connectivity in regions associated with memory functioning and executive control was reduced in patients with AN during the retrieval of specific food/body-related AM. Finally, resting-state functional connectivity analysis revealed no differences between groups, arguing against a general underlying disconnection of brain networks implicated in memory and emotional processing in AN.

Conclusions

These results indicate impaired neural processing of food/body-related AM in AN, with a reduced involvement of regions involved in self-referential processing. Our findings are discussed as possible neuronal correlates of emotional avoidance in AN and provide new insights of AN-pathophysiology underscoring the importance of targeting dysfunctional emotion regulation strategies during treatment.

Keywords

Anorexia nervosaautobiographical memoryeating disorderfMRIself-referential processing
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 3 , February 2023 , pp. 844 - 854
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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.)

Article purchase

Temporarily unavailable

Footnotes

*

Valentin Terhoeven and Christoph Nikendei contributed equally.

References

Abler, B., & Kessler, H. (2009). Emotion regulation questionnaire–Eine deutschsprachige Fassung des ERQ von Gross und John. Diagnostica, 55(3), 144–152.CrossRefGoogle Scholar
American Psychiatric Association, (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). Washington, DC: American Psychiatric Pub.CrossRefGoogle Scholar
Arastéh, K., Baenkler, H., & Bieber, C. (2018). DR Innere Medizin (4. Auflage). Stuttgart: Georg Thieme Verlag KG.Google Scholar
Arcelus, J., Mitchell, A. J., Wales, J., & Nielsen, S. (2011). Mortality rates in patients with anorexia nervosa and other eating disorders. A meta-analysis of 36 studies. Archives of General Psychiatry, 68(7), 724–731. doi: 10.1001/archgenpsychiatry.2011.74.CrossRefGoogle ScholarPubMed
Barbey, A. K., Koenigs, M., & Grafman, J. (2013). Dorsolateral prefrontal contributions to human working memory. Cortex, 49(5), 1195–1205. doi: 10.1016/j.cortex.2012.05.022.CrossRefGoogle ScholarPubMed
Bischoff-Grethe, A., Wierenga, C. E., Berner, L. A., Simmons, A. N., Bailer, U., Paulus, M. P., & Kaye, W. H. (2018). Neural hypersensitivity to pleasant touch in women remitted from anorexia nervosa. Translational Psychiatry, 8(1), 161. doi: 10.1038/s41398-018-0218-3.CrossRefGoogle ScholarPubMed
Boehm, I., Geisler, D., King, J. A., Ritschel, F., Seidel, M., Deza Araujo, Y., … Ehrlich, S. (2014). Increased resting state functional connectivity in the fronto-parietal and default mode network in anorexia nervosa. Frontiers in Behavioral Neuroscience, 8, 346. doi: 10.3389/fnbeh.2014.00346.CrossRefGoogle ScholarPubMed
Bomba, M., Marfone, M., Brivio, E., Oggiano, S., Broggi, F., Neri, F., & Nacinovich, R. (2014). Autobiographical memory in adolescent girls with anorexia nervosa. European Eating Disorders Review, 22(6), 479–486. doi: 10.1002/erv.2321.CrossRefGoogle ScholarPubMed
Bonnici, H. M., Cheke, L. G., Green, D. A. E., FitzGerald, T., & Simons, J. S. (2018). Specifying a causal role for angular gyrus in autobiographical memory. Journal of Neuroscience, 38(49), 10438–10443. doi: 10.1523/JNEUROSCI.1239-18.2018.CrossRefGoogle ScholarPubMed
Brockmeyer, T., Grosse Holtforth, M., Bents, H., Herzog, W., & Friederich, H. C. (2013). Lower body weight is associated with less negative emotions in sad autobiographical memories of patients with anorexia nervosa. Psychiatry Research, 210(2), 548–552. doi:10.1016/j.psychres.2013.06.024.CrossRefGoogle ScholarPubMed
Brockmeyer, T., Skunde, M., Wu, M., Bresslein, E., Rudofsky, G., Herzog, W., & Friederich, H. C. (2014). Difficulties in emotion regulation across the spectrum of eating disorders. Comprehensive Psychiatry, 55(3), 565–571. doi:10.1016/j.comppsych.2013.12.001.CrossRefGoogle ScholarPubMed
Calhoun, V. D., Adali, T., Pearlson, G. D., & Pekar, J. J. (2001). A method for making group inferences from functional MRI data using independent component analysis. Human Brain Mapping, 14(3), 140–151.CrossRefGoogle ScholarPubMed
Compère, L., Sperduti, M., Gallarda, T., Anssens, A., Lion, S., Delhommeau, M., … Piolino, P. (2016). Sex differences in the neural correlates of specific and general autobiographical memory. Frontiers in Human Neuroscience, 10, 285. doi: 10.3389/fnhum.2016.00285.CrossRefGoogle ScholarPubMed
Conway, M. A. (2005). Memory and the self. Journal of Memory and Language, 53(4), 594–628.CrossRefGoogle Scholar
Dalgleish, T., Williams, J. M., Golden, A. M., Perkins, N., Barrett, L. F., Barnard, P. J., … Watkins, E. (2007). Reduced specificity of autobiographical memory and depression: The role of executive control. Journal of Experimental Psychology: General, 136(1), 23–42. doi: 10.1037/0096-3445.136.1.23.CrossRefGoogle ScholarPubMed
Fossati, P. (2013). Imaging autobiographical memory. Dialogues in Clinical Neuroscience, 15(4), 487–490. doi: 10.31887/DCNS.2013.15.4/pfossati.CrossRefGoogle ScholarPubMed
Freton, M., Lemogne, C., Bergouignan, L., Delaveau, P., Lehéricy, S., & Fossati, P. (2014). The eye of the self: Precuneus volume and visual perspective during autobiographical memory retrieval. Brain Structure and Function, 219(3), 959–968. doi: 10.1007/s00429-013-0546-2.CrossRefGoogle ScholarPubMed
Friederich, H. C., Brockmeyer, T., Wild, B., Resmark, G., de Zwaan, M., Dinkel, A., … Herzog, W. (2017). Emotional expression predicts treatment outcome in focal psychodynamic and cognitive behavioural therapy for anorexia nervosa: Findings from the ANTOP study. Psychotherapy and Psychosomatics, 86(2), 108–110. doi: 10.1159/000453582.CrossRefGoogle ScholarPubMed
Gaudio, S., Wiemerslage, L., Brooks, S. J., & Schioth, H. B. (2016). A systematic review of resting-state functional-MRI studies in anorexia nervosa: Evidence for functional connectivity impairment in cognitive control and visuospatial and body-signal integration. Neuroscience and Biobehavioral Reviews, 71, 578–589. doi: 10.1016/j.neubiorev.2016.09.032.CrossRefGoogle ScholarPubMed
Härting, C., Markowitsch, H., Neufeld, H., Calabrese, P., Deisinger, K., & Kessler, J. (2000). Deutsche Adaptation der revidierten Fassung der Wechsler-Memory Scale (WMS-R). Bern, Göttingen: Verlag Hans Huber.Google Scholar
Herzog, W., Friederich, H., Wild, B., Lowe, B., & Zipfel, S. (2006). Magersucht. Therapeutische Umschau, 63(8), 539–544.CrossRefGoogle Scholar
Hilbert, A., Tuschen-Caffier, B., Karwautz, A., Niederhofer, H., & Munsch, S. (2007). Eating disorder examination-questionnaire: Psychometric properties of the German version. Diagnostica, 53(3), 144–154. doi: 10.1026/0012-1924.53.3.144.CrossRefGoogle Scholar
Huber, J., Salatsch, C., Ingenerf, K., Schmid, C., Maatouk, I., Weisbrod, M., … Nikendei, C. (2015). Characteristics of disorder-related autobiographical memory in acute anorexia nervosa patients. European Eating Disorders Review, 23(5), 379–389. doi: 10.1002/erv.2379.CrossRefGoogle ScholarPubMed
Khalsa, S. S., Craske, M. G., Li, W., Vangala, S., Strober, M., & Feusner, J. D. (2015). Altered interoceptive awareness in anorexia nervosa: Effects of meal anticipation, consumption and bodily arousal. International Journal of Eating Disorders, 48(7), 889–897. doi: 10.1002/eat.22387.CrossRefGoogle ScholarPubMed
Kim, K. R., Ku, J., Lee, J. H., Lee, H., & Jung, Y. C. (2012). Functional and effective connectivity of anterior insula in anorexia nervosa and bulimia nervosa. Neuroscience Letters, 521(2), 152–157. doi: 10.1016/j.neulet.2012.05.075.CrossRefGoogle ScholarPubMed
Köhle, K., Herzog, W., Joraschky, P., Kruse, J., Langewitz, W., & Söllner, W. (2016). Uexküll, Psychosomatische Medizin. München: Elsevier.Google Scholar
Kroenke, K., & Spitzer, R. L. (2002). The PHQ-9: A new depression diagnostic and severity measure. Psychiatric Annals, 32(9), 509–515. doi: 10.3928/0048-5713-20020901-06.CrossRefGoogle Scholar
Lehrl, S., & Merz, J. (1989). Mehrfachwahl-Wortschatz-Intelligenztest (MWT-B)(Multiple Choice Vocabulary Intelligence Test). Erlangen: Perimed.Google Scholar
Morel, N., Villain, N., Rauchs, G., Gaubert, M., Piolino, P., Landeau, B., … Chételat, G. (2014). Brain activity and functional coupling changes associated with self-reference effect during both encoding and retrieval. PLoS ONE, 9(3), e90488. doi: 10.1371/journal.pone.0090488.CrossRefGoogle ScholarPubMed
Moriguchi, Y., & Komaki, G. (2013). Neuroimaging studies of alexithymia: Physical, affective, and social perspectives. Biopsychosocial Medicine, 7(1), 8. doi: 10.1186/1751-0759-7-8.CrossRefGoogle ScholarPubMed
Nandrino, J. L., Doba, K., Lesne, A., Christophe, V., & Pezard, L. (2006). Autobiographical memory deficit in anorexia nervosa: Emotion regulation and effect of duration of illness. Journal of Psychosomatic Research, 61(4), 537–543. doi: 10.1016/j.jpsychores.2006.02.008.CrossRefGoogle ScholarPubMed
Oldershaw, A., Lavender, T., Sallis, H., Stahl, D., & Schmidt, U. (2015). Emotion generation and regulation in anorexia nervosa: A systematic review and meta-analysis of self-report data. Clinical Psychology Review, 39, 83–95. doi: 10.1016/j.cpr.2015.04.005.CrossRefGoogle ScholarPubMed
Phillipou, A., Abel, L. A., Castle, D. J., Hughes, M. E., Nibbs, R. G., Gurvich, C., & Rossell, S. L. (2016). Resting state functional connectivity in anorexia nervosa. Psychiatry Research Neuroimaging, 251, 45–52. doi: 10.1016/j.pscychresns.2016.04.008.CrossRefGoogle ScholarPubMed
Racine, S. E., & Wildes, J. E. (2015). Dynamic longitudinal relations between emotion regulation difficulties and anorexia nervosa symptoms over the year following intensive treatment. Journal of Consulting and Clinical Psychology, 83(4), 785–795. doi:10.1037/ccp0000011.CrossRefGoogle ScholarPubMed
Reitan, R. M. (1958). Validity of the trail making test as an indicator of organic brain damage. Perceptual and Motor Skills, 8(3), 271–276. doi:10.2466/pms.1958.8.3.271.CrossRefGoogle Scholar
Santel, S., Baving, L., Krauel, K., Munte, T. F., & Rotte, M. (2006). Hunger and satiety in anorexia nervosa: fMRI during cognitive processing of food pictures. Brain Research, 1114(1), 138–148. doi: 10.1016/j.brainres.2006.07.045.CrossRefGoogle ScholarPubMed
Schmidt, U., & Treasure, J. (2006). Anorexia nervosa: Valued and visible. A cognitive-interpersonal maintenance model and its implications for research and practice. British Journal of Clinical Psychology, 45(Pt 3), 343–366.CrossRefGoogle ScholarPubMed
Simon, J. J., Stopyra, M. A., & Friederich, H. C. (2019). Neural processing of disorder-related stimuli in patients with anorexia nervosa: A narrative review of brain imaging studies. Journal of Clinical Medicine, 8(7), 1047. doi: 10.3390/jcm8071047.CrossRefGoogle ScholarPubMed
Spielberger, C. D. (2010). State-Trait anxiety inventory. In Weiner, I. B., & Craighead, W. E. (Eds.), The Corsini Encyclopedia of Psychology. Hoboken: John Wiley & Sons, Inc.. Available at https://onlinelibrary.wiley.com/doi/full/10.1002/9780470479216.corpsy0943Google Scholar
Sreekumar, V., Nielson, D. M., Smith, T. A., Dennis, S. J., & Sederberg, P. B. (2018). The experience of vivid autobiographical reminiscence is supported by subjective content representations in the precuneus. Scientific Reports, 8(1), 14899. doi: 10.1038/s41598-018-32879-0.CrossRefGoogle ScholarPubMed
Stunkard, A. J., & Messick, S. (1985). The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. Journal of Psychosomatic Research, 29(1), 71–83.CrossRefGoogle ScholarPubMed
Thome, J., Terpou, B. A., McKinnon, M. C., & Lanius, R. A. (2020). The neural correlates of trauma-related autobiographical memory in posttraumatic stress disorder: A meta-analysis. Depression and Anxiety, 37(4), 321–345. doi: 10.1002/da.22977.CrossRefGoogle ScholarPubMed
Treasure, J., & Schmidt, U. (2013). The cognitive-interpersonal maintenance model of anorexia nervosa revisited: A summary of the evidence for cognitive, socio-emotional and interpersonal predisposing and perpetuating factors. Journal of Eating Disorders, 1, 13. doi: 10.1186/2050-2974-1-13.CrossRefGoogle ScholarPubMed
Uher, R., Murphy, T., Brammer, M. J., Dalgleish, T., Phillips, M. L., Ng, V. W., … Treasure, J. (2004). Medial prefrontal cortex activity associated with symptom provocation in eating disorders. American Journal of Psychiatry, 161(7), 1238–1246.CrossRefGoogle ScholarPubMed
Vocks, S., Busch, M., Gronemeyer, D., Schulte, D., Herpertz, S., & Suchan, B. (2010). Neural correlates of viewing photographs of one's own body and another woman's body in anorexia and bulimia nervosa: An fMRI study. Journal of Psychiatry and Neuroscience, 35(3), 163–176.CrossRefGoogle ScholarPubMed
Weschler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). London: Psychological Corporation.Google Scholar
Williams, J. M., Barnhofer, T., Crane, C., Herman, D., Raes, F., Watkins, E., & Dalgleish, T. (2007). Autobiographical memory specificity and emotional disorder. Psychological Bulletin, 133(1), 122–148. doi: 10.1037/0033-2909.133.1.122.CrossRefGoogle ScholarPubMed
Young, K. D., Bellgowan, P. S., Bodurka, J., & Drevets, W. C. (2013). Behavioral and neurophysiological correlates of autobiographical memory deficits in patients with depression and individuals at high risk for depression. JAMA Psychiatry, 70(7), 698–708. doi: 10.1001/jamapsychiatry.2013.1189.CrossRefGoogle ScholarPubMed
Young, K. D., Bellgowan, P. S., Bodurka, J., & Drevets, W. C. (2014). Neurophysiological correlates of autobiographical memory deficits in currently and formerly depressed subjects. Psychological Medicine, 44(14), 2951–2963. doi: 10.1017/S0033291714000464.CrossRefGoogle ScholarPubMed
Young, K. D., Drevets, W. C., Bodurka, J., & Preskorn, S. S. (2016). Amygdala activity during autobiographical memory recall as a biomarker for residual symptoms in patients remitted from depression. Psychiatry Research Neuroimaging, 248, 159–161. doi: 10.1016/j.pscychresns.2016.01.017.CrossRefGoogle ScholarPubMed
Zhu, Y., Hu, X., Wang, J., Chen, J., Guo, Q., Li, C., & Enck, P. (2012). Processing of food, body and emotional stimuli in anorexia nervosa: A systematic review and meta-analysis of functional magnetic resonance imaging studies. European Eating Disorders Review, 20(6), 439–450. doi: 10.1002/erv.2197.CrossRefGoogle ScholarPubMed
Zipfel, S., Lowe, B., Reas, D. L., Deter, H. C., & Herzog, W. (2000). Long-term prognosis in anorexia nervosa: Lessons from a 21-year follow-up study. Lancet (London, England), 355(9205), 721–722. doi: 10.1016/S0140-6736(99)05363-5.CrossRefGoogle ScholarPubMed
Supplementary material: File

Terhoeven et al. supplementary material

Terhoeven et al. supplementary material

Download Terhoeven et al. supplementary material(File)
File 1 MB