Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-24T01:02:58.874Z Has data issue: false hasContentIssue false

Subliminal and supraliminal processing of reward-related stimuli in anorexia nervosa

Published online by Cambridge University Press:  23 August 2017

I. Boehm
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
J. A. King
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
F. Bernardoni
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
D. Geisler
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
M. Seidel
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
F. Ritschel
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
T. Goschke
Affiliation:
Department of Psychology, Technische Universität Dresden, Dresden, Germany
J.-D. Haynes
Affiliation:
Bernstein Center for Computational Neuroscience, Charité Universitäts-Medizin, Berlin, Germany
V. Roessner
Affiliation:
Department of Child and Adolescent Psychiatry, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
S. Ehrlich*
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany Department of Child and Adolescent Psychiatry, Eating Disorders Research and Treatment Center, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
*
*Address for correspondence: S, Ehrlich, M.D., Division of Psychological and Social Medicine and Developmental Neurosciences, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany and Translational Developmental Neuroscience Section, Fetscherstraße 74, Dresden 01307, Germany. (Email: [email protected])

Abstract

Background

Previous studies have highlighted the role of the brain reward and cognitive control systems in the etiology of anorexia nervosa (AN). In an attempt to disentangle the relative contribution of these systems to the disorder, we used functional magnetic resonance imaging (fMRI) to investigate hemodynamic responses to reward-related stimuli presented both subliminally and supraliminally in acutely underweight AN patients and age-matched healthy controls (HC).

Methods

fMRI data were collected from a total of 35 AN patients and 35 HC, while they passively viewed subliminally and supraliminally presented streams of food, positive social, and neutral stimuli. Activation patterns of the group×stimulation condition×stimulus type interaction were interrogated to investigate potential group differences in processing different stimulus types under the two stimulation conditions. Moreover, changes in functional connectivity were investigated using generalized psychophysiological interaction analysis.

Results

AN patients showed a generally increased response to supraliminally presented stimuli in the inferior frontal junction (IFJ), but no alterations within the reward system. Increased activation during supraliminal stimulation with food stimuli was observed in the AN group in visual regions including superior occipital gyrus and the fusiform gyrus/parahippocampal gyrus. No group difference was found with respect to the subliminal stimulation condition and functional connectivity.

Conclusion

Increased IFJ activation in AN during supraliminal stimulation may indicate hyperactive cognitive control, which resonates with clinical presentation of excessive self-control in AN patients. Increased activation to food stimuli in visual regions may be interpreted in light of an attentional food bias in AN.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2017 

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

Ashburner, J (2007). A fast diffeomorphic image registration algorithm. Neuroimage 38, 95113.Google Scholar
Baars, BJ (2002). The conscious access hypothesis: origins and recent evidence. Trends in Cognitive Sciences 6, 4752.Google Scholar
Baldauf, D, Desimone, R (2014). Neural mechanisms of object-based attention. Science 344, 424427.CrossRefGoogle ScholarPubMed
Berridge, KC, Kringelbach, ML (2015). Pleasure systems in the brain. Neuron 86, 646664.Google Scholar
Bischoff-Grethe, A, McCurdy, D, Grenesko-Stevens, E, Irvine, LE, Wagner, A, Wendy Yau, W-Y, Fennema-Notestine, C, Wierenga, CE, Fudge, JL, Delgado, MR (2013). Altered brain response to reward and punishment in adolescents with anorexia nervosa. Psychiatry Research: Neuroimaging 214, 331340.Google Scholar
Blundell, J, De Graaf, C, Hulshof, T, Jebb, S, Livingstone, B, Lluch, A, Mela, D, Salah, S, Schuring, E, Van Der Knaap, H, Westerterp, M (2010). Appetite control: methodological aspects of the evaluation of foods. Obesity Reviews 11, 251270.Google Scholar
Botvinick, M, Braver, T (2015). Motivation and cognitive control: from behavior to neural mechanism. Annual Review of Psychology 66, 83113.CrossRefGoogle ScholarPubMed
Botvinick, MM, Cohen, JD (2014). The computational and neural basis of cognitive control: charted territory and new frontiers. Cognitive science 38, 12491285.CrossRefGoogle ScholarPubMed
Brass, M, Derrfuss, J, Forstmann, B, von Cramon, DY (2005). The role of the inferior frontal junction area in cognitive control. Trends in Cognitive Sciences 9, 314316.Google Scholar
Brett, M, Anton, J, Valabregue, R, Poline, J (2002). Region of interest analysis using an SPM toolbox. Paper presented at 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.Google Scholar
Brooks, S, O'Daly, O, Uher, R, Schiöth, H, Treasure, J, Campbell, I (2012a). Subliminal food images compromise superior working memory performance in women with restricting anorexia nervosa. Consciousness and Cognition 21, 751763.CrossRefGoogle ScholarPubMed
Brooks, S, Owen, G, Uher, R, Friederich, H, Giampietro, V, Brammer, M, Williams, S, Schiöth, H, Treasure, J, Campbell, I (2011a). Differential neural responses to food images in women with bulimia versus anorexia nervosa. PLoS ONE 6, e22259.Google Scholar
Brooks, S, Prince, A, Stahl, D, Campbell, I, Treasure, J (2011b). A systematic review and meta-analysis of cognitive bias to food stimuli in people with disordered eating behaviour. Clinical Psychology Review 31, 3751.CrossRefGoogle ScholarPubMed
Brooks, SJ, Savov, V, Allzén, E, Benedict, C, Fredriksson, R, Schiöth, HB (2012b). Exposure to subliminal arousing stimuli induces robust activation in the amygdala, hippocampus, anterior cingulate, insular cortex and primary visual cortex: a systematic meta-analysis of fMRI studies. NeuroImage 59, 29622973.Google Scholar
Camus, M, Halelamien, N, Plassmann, H, Shimojo, S, O'Doherty, J, Camerer, C, Rangel, A (2009). Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices. European Journal of Neuroscience 30, 19801988.Google Scholar
Childress, AR, Ehrman, RN, Wang, Z, Li, Y, Sciortino, N, Hakun, J, Jens, W, Suh, J, Listerud, J, Marquez, K, Franklin, T, Langleben, D, Detre, J, O'Brien, CP (2008). Prelude to passion: limbic activation by ‘unseen’ drug and sexual cues. PLoS ONE 3, e1506.Google Scholar
Cole, MW, Repovš, G, Anticevic, A (2014). The frontoparietal control system A central role in mental health. The Neuroscientist 20, 652664.Google Scholar
Cowdrey, FA, Park, RJ, Harmer, CJ, McCabe, C (2011). Increased neural processing of rewarding and aversive food stimuli in recovered anorexia nervosa. Biological Psychiatry 70, 736743.Google Scholar
Dehaene, S, Changeux, J-P, Naccache, L, Sackur, J, Sergent, C (2006). Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends in Cognitive Sciences 10, 204211.Google Scholar
Derrfuss, J, Brass, M, Neumann, J, von Cramon, DY (2005). Involvement of the inferior frontal junction in cognitive control: meta-analyses of switching and stroop studies. Human Brain Mapping 25, 2234.Google Scholar
Dickson, H, Brooks, S, Uher, R, Tchanturia, K, Treasure, J, Campbell, I (2008). The inability to ignore: distractibility in women with restricting anorexia nervosa. Psychological Medicine 38, 17411748.Google Scholar
Ehrlich, S, Geisler, D, Ritschel, F, King, JA, Seidel, M, Boehm, I, Breier, M, Clas, S, Weiss, J, Marxen, M, Smolka, MN, Roessner, V, Kroemer, NB (2015). Elevated cognitive control over reward processing in recovered patients with anorexia nervosa. Journal of Psychiatry and Neuroscience 40, 307315.Google Scholar
Fichter, M, Quadflieg, N (1999). SIAB. Struckturiertes Inventar Fuer Anorektische und Bulimische Essstoerungen Nach DSM-IV und ICD-10. Huber: Bern.Google Scholar
Foerde, K, Steinglass, JE, Shohamy, D, Walsh, BT (2015). Neural mechanisms supporting maladaptive food choices in anorexia nervosa. Nature Neuroscience 18, 15711573.Google Scholar
Frank, G, Shott, ME, Hagman, JO, Mittal, VA (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, 11521160.CrossRefGoogle ScholarPubMed
Goschke, T (2014). Dysfunctions of decision-making and cognitive control as transdiagnostic mechanisms of mental disorders: advances, gaps, and needs in current research. International Journal of Methods in Psychiatric Research 23, 4157.CrossRefGoogle ScholarPubMed
Hacker, MJ, Ratcliff, R (1979). A revised table of d’ for M-alternative forced choice. Perception & Psychophysics 26, 168170.Google Scholar
Hare, TA, Camerer, CF, Rangel, A (2009). Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324, 646648.Google Scholar
Heatherton, TF, Wagner, DD (2011). Cognitive neuroscience of self-regulation failure. Trends in Cognitive Sciences 15, 132139.Google Scholar
Joos, AAB, Saum, B, van Elst, LT, Perlov, E, Glauche, V, Hartmann, A, Freyer, T, Tüscher, O, Zeeck, A (2011). Amygdala hyperreactivity in restrictive anorexia nervosa. Psychiatry Research: Neuroimaging 191, 189195.Google Scholar
Kaye, W, Fudge, J, Paulus, M (2009). New insights into symptoms and neurocircuit function of anorexia nervosa. Nature Reviews Neuroscience 10, 573584.Google Scholar
Kim, KR, 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, 152157.Google Scholar
King, JA, Geisler, D, Bernardoni, F, Ritschel, F, Böhm, I, Seidel, M, Mennigen, E, Ripke, S, Smolka, MN, Roessner, V, Ehrlich, S (2016). Altered neural efficiency of decision making during temporal reward discounting in anorexia nervosa. Journal of the American Academy of Child & Adolescent Psychiatry 55, 972979.Google Scholar
Kroemer, NB, Krebs, L, Kobiella, A, Grimm, O, Vollstädt-Klein, S, Wolfensteller, U, Kling, R, Bidlingmaier, M, Zimmermann, US, Smolka, MN (2013). (Still) longing for food: insulin reactivity modulates response to food pictures. Human Brain Mapping 34, 23672380.Google Scholar
Lang, PJ, Bradley, MM, Cuthbert, BN (1999). International Affective Picture System (IAPS): Instruction Manual and Affective Ratings, vol. 2. Center of Research in Psychophysiology, University of Florida: Gainesville, Florida, USA.Google Scholar
Lopez, C, Tchanturia, K, Stahl, D, Booth, R, Holliday, J, Treasure, J (2008). An examination of the concept of central coherence in women with anorexia nervosa. The International Journal of Eating Disorders 41, 143152.Google Scholar
McAdams, CJ, Lohrenz, T, Montague, PR (2015). Neural responses to kindness and malevolence differ in illness and recovery in women with anorexia nervosa. Human Brain Mapping 36, 52075219.CrossRefGoogle ScholarPubMed
McClelland, J, Bozhilova, N, Nestler, S, Campbell, IC, Jacob, S, Johnson-Sabine, E, Schmidt, U (2013). Improvements in symptoms following neuronavigated repetitive transcranial magnetic stimulation (rTMS) in severe and enduring anorexia nervosa: findings from two case studies. European Eating Disorders Review 21, 500506.CrossRefGoogle ScholarPubMed
McLaren, DG, Ries, ML, Xu, G, Johnson, SC (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61, 12771286.Google Scholar
Meneguzzo, P, Tsakiris, M, Schioth, HB, Stein, DJ, Brooks, SJ (2014). Subliminal versus supraliminal stimuli activate neural responses in anterior cingulate cortex, fusiform gyrus and insula: a meta-analysis of fMRI studies. BMC Psychology 2, 5263.Google Scholar
Miller, EK, Cohen, JD (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167202.CrossRefGoogle ScholarPubMed
Mudrik, L, Faivre, N, Koch, C (2014). Information integration without awareness. Trends in Cognitive Sciences 18, 488496.Google Scholar
O'Hara, CB, Campbell, IC, Schmidt, U (2015). A reward-centred model of anorexia nervosa: a focussed narrative review of the neurological and psychophysiological literature. Neuroscience & Biobehavioral Reviews 52, 131152.Google Scholar
Paul, T, Thiel, A (2005). Eating Disorder Inventory-2 (EDI-2): Deutsche Version. Hogrefe: Goettingen.Google Scholar
Pop-Jordanova, N (2000). Psychological characteristics and biofeedback mitigation in preadolescents with eating disorders. Pediatrics International 42, 7681.CrossRefGoogle ScholarPubMed
Sackville, T, Schotte, DE, Touyz, SW, Griffiths, R, Beumont, P (1998). Conscious and preconscious processing of food, body weight and shape, and emotion-related words in women with anorexia nervosa. International Journal of Eating Disorders 23, 7782.Google Scholar
Sanders, N, Smeets, PA, van Elburg, AA, Danner, UN, van Meer, F, Hoek, HW, Adan, RA (2015). Altered food-cue processing in chronically ill and recovered women with anorexia nervosa. Frontiers in Behavioral Neuroscience 9, 46.Google Scholar
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, 343366.CrossRefGoogle ScholarPubMed
Seeley, WW, Menon, V, Schatzberg, AF, Keller, J, Glover, GH, Kenna, H, Reiss, AL, Greicius, MD (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience 27, 23492356.Google Scholar
Shafran, R, Lee, M, Cooper, Z, Palmer, R, Fairburn, C (2007). Attentional bias in eating disorders. International Journal of Eating Disorders 40, 369380.CrossRefGoogle ScholarPubMed
Steinglass, JE, Walsh, BT (2016). Neurobiological model of the persistence of anorexia nervosa. Journal of Eating Disorders 39, 267275.Google Scholar
Sundermann, B, Pfleiderer, B (2012). Functional connectivity profile of the human inferior frontal junction: involvement in a cognitive control network. BMC Neuroscience 13, 119.Google Scholar
Toffoletto, S, Lanzenberger, R, Gingnell, M, Sundström-Poromaa, I, Comasco, E (2014). Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology 50, 2852.Google Scholar
Via, E, Soriano-Mas, C, Sánchez, I, Forcano, L, Harrison, BJ, Davey, CG, Pujol, J, Martínez-Zalacaín, I, Menchón, JM, Fernández-Aranda, F, Cardoner, N (2015). Abnormal social reward responses in anorexia nervosa: an fMRI study. PLoS ONE 10, e0133539.Google Scholar
Wagner, A, Aizenstein, H, Mazurkewicz, L, Fudge, J, Frank, G, Putnam, K, Bailer, U, Fischer, L, Kaye, W (2007a). Altered insula response to taste stimuli in individuals recovered from restricting-type anorexia nervosa. Neuropsychopharmacology 33, 513523.Google Scholar
Wagner, A, Aizenstein, H, Venkatraman, V, Fudge, J, May, J, Mazurkewicz, L, Frank, G, Bailer, U, Fischer, L, Nguyen, V (2007b). Altered reward processing in women recovered from anorexia nervosa. American Journal of Psychiatry 164, 18421849.Google Scholar
Walsh, BT (2013). The enigmatic persistence of anorexia nervosa. The American Journal of Psychiatry 170, 477484.CrossRefGoogle ScholarPubMed
Wang, KS, Smith, DV, Delgado, MR (2016). Using fMRI to study reward processing in humans: past, present, and future. Journal of Neurophysiology 115, 16641678.Google Scholar
Wessa, M, Kanske, P, Neumeister, P, Bode, K, Heissler, J, Schönfelder, S (2010). Emopics: subjektive und psychophysiologische evaluation neuen bildmaterials für die klinisch-biopsychologische forschung. Available from Michele Wessa, Google Scholar
Whitfield-Gabrieli, S, Thermenos, HW, Milanovic, S, Tsuang, MT, Faraone, SV, McCarley, RW, Shenton, ME, Green, AI, Nieto-Castanon, A, LaViolette, P (2009). Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 106, 12791284.CrossRefGoogle ScholarPubMed
Wierenga, CE, Bischoff-Grethe, A, Melrose, AJ, Irvine, Z, Torres, L, Bailer, UF, Simmons, A, Fudge, JL, McClure, SM, Ely, A, Kaye, WH (2015). Hunger does not motivate reward in women remitted from anorexia nervosa. Biological Psychiatry 77, 642652.Google Scholar
Wildes, JE, Marcus, MD (2011). Development of emotion acceptance behavior therapy for anorexia nervosa: a case series. International Journal of Eating Disorders 44, 421427.Google Scholar
Xu, Y (2014). Inferior frontal junction biases perception through neural synchrony. Trends in Cognitive Sciences 18, 447448.Google Scholar
Zanto, TP, Rubens, MT, Bollinger, J, Gazzaley, A (2010). Top-down modulation of visual feature processing: the role of the inferior frontal junction. NeuroImage 53, 736745.CrossRefGoogle ScholarPubMed
Zedelius, CM, Veling, H, Aarts, H (2011). Boosting or choking–how conscious and unconscious reward processing modulate the active maintenance of goal-relevant information. Consciousness and Cognition 20, 355362.CrossRefGoogle ScholarPubMed
Supplementary material: File

Boehm et al supplementary material

Boehm et al supplementary material 1

Download Boehm et al supplementary material(File)
File 1.3 MB