Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-19T09:05:49.420Z Has data issue: false hasContentIssue false
  • English
  • Français

Restrictive eating across a spectrum from healthy to unhealthy: behavioral and neural mechanisms

Published online by Cambridge University Press:  13 October 2020

Karin Foerde Open the ORCID record for Karin Foerde [Opens in a new window] ,
Janet E. Schebendach ,
Lauren Davis ,
Nathaniel Daw ,
B. Timothy Walsh ,
Daphna Shohamy  and
Joanna E. Steinglass
Karin Foerde*
Affiliation:
Department of Psychiatry, New York State Psychiatric Institute, New York, USA Department of Psychiatry, Columbia University Irving Medical Center, New York, USA
Janet E. Schebendach
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center, New York, USA
Lauren Davis
Affiliation:
Department of Psychiatry, New York State Psychiatric Institute, New York, USA
Nathaniel Daw
Affiliation:
Department of Psychology, Princeton Neuroscience Institute, Princeton University, Princeton, USA
B. Timothy Walsh
Affiliation:
Department of Psychiatry, New York State Psychiatric Institute, New York, USA Department of Psychiatry, Columbia University Irving Medical Center, New York, USA
Daphna Shohamy
Affiliation:
Psychology Department and Zuckerman Mind Brain and Behavior Institute, Columbia University, New York, USA
Joanna E. Steinglass
Affiliation:
Department of Psychiatry, New York State Psychiatric Institute, New York, USA Department of Psychiatry, Columbia University Irving Medical Center, New York, USA
*
Author for correspondence: Karin Foerde, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Restriction of food intake is a central feature of anorexia nervosa (AN) and other eating disorders, yet also occurs in the absence of psychopathology. The neural mechanisms of restrictive eating in health and disease are unclear.

Methods

This study examined behavioral and neural mechanisms associated with restrictive eating among individuals with and without eating disorders. Dietary restriction was examined in four groups of women (n = 110): healthy controls, dieting healthy controls, patients with subthreshold (non-low weight) AN, and patients with AN. A Food Choice Task was administered during fMRI scanning to examine neural activation associated with food choices, and a laboratory meal was conducted.

Results

Behavioral findings distinguished between healthy and ill participants. Healthy individuals, both dieting and non-dieting, chose significantly more high-fat foods than patients with AN or subthreshold AN. Among healthy individuals, choice was primarily influenced by tastiness, whereas, among both patient groups, healthiness played a larger role. Dorsal striatal activation associated with choice was most pronounced among individuals with AN and was significantly associated with selecting fewer high-fat choices in the task and lower caloric intake in the meal the following day.

Conclusions

A continuous spectrum of behavior was suggested by the increasing amount of weight loss across groups. Yet, data from this Food Choice Task with fMRI suggest there is a behavioral distinction between illness and health, and that the neural mechanisms underlying food choice in AN are distinct. These behavioral and neural mechanisms of restrictive eating may be useful targets for treatment development.

Keywords

anorexia nervosacognitive neurosciencedecision-makingfood choicefMRIneuroimaging
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 9 , July 2022 , pp. 1755 - 1764
Check for updates
Copyright
Copyright © The Author(s), 2020. 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.)

References

American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders: Fifth edition (DSM-5). Washington, DC: American Psychiatric Association.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.CrossRefGoogle ScholarPubMed
Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68(3), 255–278.CrossRefGoogle ScholarPubMed
Bartra, O., McGuire, J. T., & Kable, J. W. (2013). The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage, 76, 412–427.CrossRefGoogle ScholarPubMed
Bates, D., Maechler, M., & Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes. Online: http://CRAN.R-project.org/package=lme4 .Google Scholar
Beck, A. T., & Steer, R. A. (1993). Depression inventory manual. San Antonio, TX: Psychological Corporation, Harcourt, Brace.Google Scholar
Bennett, D., Silverstein, S. M., & Niv, Y. (2019). The two cultures of computational psychiatry. JAMA Psychiatry, 76(6), 563–564.CrossRefGoogle ScholarPubMed
Berner, L. A., Shaw, J. A., Witt, A. A., & Lowe, M. R. (2013). The relation of weight suppression and body mass index to symptomatology and treatment response in anorexia nervosa. Journal of Abnormal Psychology, 122(3), 694–708.CrossRefGoogle ScholarPubMed
Cloninger, C. R., Przybeck, T. R., Svrakic, D. M., & Wetzel, R. D. (1994). The temperament and character inventory (TCI): A guide to its development and Use. St. Louis, MO: Center for Psychobiology of Personality, Washington University.Google Scholar
Fairburn, C. G., & Beglin, S. J. (1994). Assessment of eating disorders: Interview or self-report questionnaire? International Journal of Eating Disorders, 16(4), 363–370.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
First, M., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1998). Structured Clinical Interview for DSM-IV Disorders. Washington, DC: American Psychiatric Press.Google Scholar
Foerde, K., Steinglass, J. E., Shohamy, D., & Walsh, B. T. (2015). Neural mechanisms supporting maladaptive food choices in anorexia nervosa. Nature Neuroscience, 18(11), 1571–1573.CrossRefGoogle ScholarPubMed
Frank, G. K. W., DeGuzman, M. C., Shott, M. E., Laudenslager, M. L., Rossi, B., & Pryor, T. (2018). Association of brain reward learning response with harm avoidance, weight gain, and hypothalamic effective connectivity in adolescent anorexia nervosa. JAMA Psychiatry, 75(10), 1071–1080.CrossRefGoogle ScholarPubMed
Frank, G. K. W., Shott, M. E., Hagman, J. O., & Mittal, V. A. (2013). Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. American Journal of Psychiatry, 170(10), 1152–1160.CrossRefGoogle ScholarPubMed
Georgii, C., Schulte-Mecklenbeck, M., Richard, A., Van Dyck, Z., & Blechert, J. (2020). The dynamics of self-control: Within-participant modeling of binary food choices and underlying decision processes as a function of restrained eating. Psychological Research, 84, 1777–1788.CrossRefGoogle ScholarPubMed
Gillan, C. M., Apergis-Schoute, A. M., Morein-Zamir, S., Urcelay, G. P., Sule, A., Fineberg, N. A., … Robbins, T. W. (2015). Functional neuroimaging of avoidance habits in obsessive-compulsive disorder. American Journal of Psychiatry, 172(3), 284–293.CrossRefGoogle ScholarPubMed
Hare, T. A., Camerer, C. F., & Rangel, A. (2009). Self-control in decision-making involves modulation of the vmPFC valuation system. Science (New York, NY), 324(5927), 646–648.CrossRefGoogle ScholarPubMed
Haynos, A. F., Hall, L. M. J., Lavender, J. M., Peterson, C. B., Crow, S. J., Klimes-Dougan, B., … Camchong, J. (2019). Resting state functional connectivity of networks associated with reward and habit in anorexia nervosa. Human Brain Mapping, 40(2), 652–662.CrossRefGoogle ScholarPubMed
Huys, Q. J., Maia, T. V., & Frank, M. J. (2016). Computational psychiatry as a bridge from neuroscience to clinical applications. Nature Neuroscience, 19(3), 404–413.CrossRefGoogle ScholarPubMed
Kable, J. W., & Glimcher, P. W. (2007). The neural correlates of subjective value during intertemporal choice. Nature Neuroscience, 10(12), 1625–1633.CrossRefGoogle ScholarPubMed
Kim, S. (2015). ppcor: An R package for a fast calculation to semi-partial correlation coefficients. Communications for Statistical Applications and Methods, 22(6), 665–674.CrossRefGoogle Scholar
King, J. A., Geisler, D., Ritschel, F., Boehm, I., Seidel, M., Roschinski, B., … Ehrlich, S. (2015). Global cortical thinning in acute anorexia nervosa normalizes following long-term weight restoration. Biological Psychiatry, 77(7), 624–632.CrossRefGoogle ScholarPubMed
Lambert, C., Da Silva, S., Ceniti, A. K., Rizvi, S. J., Foussias, G., & Kennedy, S. H. (2018). Anhedonia in depression and schizophrenia: A transdiagnostic challenge. CNS Neuroscience & Therapeutics, 24(7), 615–623.CrossRefGoogle ScholarPubMed
Liljeholm, M., & O'Doherty, J. P. (2012). Contributions of the striatum to learning, motivation, and performance: An associative account. Trends in Cognitive Sciences, 16(9), 467–475.CrossRefGoogle Scholar
Lloyd, C. E., & Steinglass, J. E. (2018). What can food-image tasks teach us about anorexia nervosa? A systematic review. Journal of Eating Disorders, 6(1), 31.CrossRefGoogle ScholarPubMed
Olivo, G., Solstrand Dahlberg, L., Wiemerslage, L., Swenne, I., Zhukovsky, C., Salonen-Ros, H., … Schioth, H. B. (2018). Atypical anorexia nervosa is not related to brain structural changes in newly diagnosed adolescent patients. International Journal of Eating Disorders, 51(1), 39–45.CrossRefGoogle Scholar
Palmiter, R. D. (2007). Is dopamine a physiologically relevant mediator of feeding behavior? Trends in Neurosciences, 30(8), 375–381.CrossRefGoogle ScholarPubMed
Palmiter, R. D. (2008). Dopamine signaling in the dorsal striatum is essential for motivated behaviors: Lessons from dopamine-deficient mice. Annals of the New York Academy of Sciences, 1129, 35–46.CrossRefGoogle ScholarPubMed
Peters, J., & Buchel, C. (2011). The neural mechanisms of inter-temporal decision-making: Understanding variability. Trends in Cognitive Sciences, 15(5), 227–239.CrossRefGoogle ScholarPubMed
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59(3), 2142–2154.CrossRefGoogle ScholarPubMed
Raatz, S. K., Jahns, L., Johnson, L. K., Crosby, R., Mitchell, J. E., Crow, S., … Wonderlich, S. A. (2015). Nutritional adequacy of dietary intake in women with anorexia nervosa. Nutrients, 7(5), 3652–3665.CrossRefGoogle ScholarPubMed
Rangel, A. (2013). Regulation of dietary choice by the decision-making circuitry. Nature Neuroscience, 16(12), 1717–1724.CrossRefGoogle ScholarPubMed
Rothemund, Y., Buchwald, C., Georgiewa, P., Bohner, G., Bauknecht, H. C., Ballmaier, M., … Klingebiel, R. (2011). Compulsivity predicts fronto striatal activation in severely anorectic individuals. Neuroscience, 197, 242–250.CrossRefGoogle ScholarPubMed
Schebendach, J. E., Mayer, L. E., Devlin, M. J., Attia, E., Contento, I. R., Wolf, R. L., & Walsh, B. T. (2008). Dietary energy density and diet variety as predictors of outcome in anorexia nervosa. The American Journal of Clinical Nutrition, 87(4), 810–816.CrossRefGoogle ScholarPubMed
Schebendach, J. E., Mayer, L. E., Devlin, M. J., Attia, E., & Walsh, B. T. (2012). Dietary energy density and diet variety as risk factors for relapse in anorexia nervosa: A replication. International Journal of Eating Disorders, 45(1), 79–84.CrossRefGoogle ScholarPubMed
Schebendach, J. E., Uniacke, B., Walsh, B. T., Mayer, L. E. S., Attia, E., & Steinglass, J. E. (2019). Fat preference and fat intake in individuals with and without anorexia nervosa. Appetite, 139, 35–41.CrossRefGoogle ScholarPubMed
Siegel, J. S., Power, J. D., Dubis, J. W., Vogel, A. C., Church, J. A., Schlaggar, B. L., & Petersen, S. E. (2014). Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high-motion data points. Human Brain Mapping, 35(5), 1981–1996.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl 1), S208–S219.CrossRefGoogle ScholarPubMed
Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, A. G. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto: Consulting Psychologists Press, Inc.Google Scholar
Steinglass, J. E., Foerde, K., Kostro, K., Shohamy, D., & Walsh, B. T. (2015). Restrictive food intake as a choice-A paradigm for study. International Journal of Eating Disorders, 48(1), 59–66.CrossRefGoogle ScholarPubMed
Steinglass, J. E., Glasofer, D. R., Dalack, M., & Attia, E. (2020). Between wellness, relapse, and remission: Stages of illness in anorexia nervosa. International Journal of Eating Disorders, 53, 1088–1096.CrossRefGoogle ScholarPubMed
Steinglass, J. E., Glasofer, D. R., Walsh, E., Guzman, G., Peterson, C. B., Walsh, B. T., … Wonderlich, S. A. (2018). Targeting habits in anorexia nervosa: A proof-of-concept randomized trial. Psychological Medicine, 48(15), 2584–2591.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
Sweitzer, M. M., Watson, K. K., Erwin, S. R., Winecoff, A. A., Datta, N., Huettel, S., … Zucker, N. L. (2018). Neurobiology of social reward valuation in adults with a history of anorexia nervosa. PLoS ONE, 13(12), e0205085.CrossRefGoogle ScholarPubMed
Sysko, R., Glasofer, D. R., Hildebrandt, T., Klimek, P., Mitchell, J. E., Berg, K. C., … Walsh, B. T. (2015). The eating disorder assessment for DSM-5 (EDA-5): Development and validation of a structured interview for feeding and eating disorders. International Journal of Eating Disorders, 48(5), 452–463.CrossRefGoogle ScholarPubMed
Sysko, R., Steinglass, J. E., Schebendach, J. E., Mayer, L. E. S., & Walsh, B. T. (2018). Rigor and reproducibility via laboratory studies of eating behavior: A focused update and conceptual review. International Journal of Eating Disorders, 51(7), 608–616.CrossRefGoogle ScholarPubMed
Sysko, R., Walsh, B. T., Schebendach, J., & Wilson, G. T. (2005). Eating behavior among women with anorexia nervosa. The American Journal of Clinical Nutrition, 82(2), 296–301.CrossRefGoogle ScholarPubMed
Uniacke, B., Slattery, R., Walsh, B. T., Shohamy, D., Foerde, K., & Steinglass, J. (2020). A comparison of food-based decision-making between restricting and binge-eating/purging subtypes of anorexia nervosa. International Journal of Eating Disorders. doi: 10.1002/eat.23359CrossRefGoogle ScholarPubMed
Walsh, B. T. (2011). The importance of eating behavior in eating disorders. Physiology & Behavior, 104(4), 525–529.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler adult intelligence scale – III. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence manual. San Antonio: The Psychological Corporation.Google Scholar
Yue, L., Wang, Y., Kaye, W. H., Kang, Q., Huang, J. B., Cheung, E. F. C., … Chan, R. C. K. (2018). Structural alterations in the caudate nucleus and precuneus in un-medicated anorexia nervosa patients. Psychiatry Research: Neuroimaging, 281, 12–18.CrossRefGoogle ScholarPubMed
Zambrowicz, R., Schebendach, J. E., Sysko, R., Mayer, L. E. S., Walsh, B. T., & Steinglass, J. E. (2019). Relationship between three factor eating questionnaire-restraint subscale and food intake. International Journal of Eating Disorders, 52(3), 255–260.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Foerde et al. Supplementary Materials

Foerde et al. Supplementary Materials

Download Foerde et al. Supplementary Materials(PDF)
PDF 5.3 MB