Abstract
Trichotillomania (hair pulling disorder) and skin picking disorder are common and often debilitating mental health conditions, grouped under the umbrella term of body focused repetitive behaviors (BFRBs). Although the pathophysiology of BFRBs is incompletely understood, reward processing dysfunction has been implicated in the etiology and sustention of these disorders. The purpose of this study was to probe reward processing in BFRBs. 159 adults (125 with a BFRB [83.2% (n = 104) female] and 34 healthy controls [73.5% (n = 25) female]) were recruited from the community for a multi-center between-group comparison using a functional imaging (fMRI) monetary reward task. Differences in brain activation during reward anticipation and punishment anticipation were compared between BFRB patients and controls, with stringent correction for multiple comparisons. All group level analyses controlled for age, sex and scanning site. Compared to controls, BFRB participants showed marked hyperactivation of the bilateral inferior frontal gyrus (pars opercularis and pars triangularis) compared to controls. In addition, BFRB participants exhibited increased activation in multiple areas during the anticipation of loss (right fusiform gyrus, parahippocampal gyrus, cerebellum, right inferior parietal lobule; left inferior frontal gyrus). There were no significant differences in the win-lose contrast between the two groups. These data indicate the existence of dysregulated reward circuitry in BFRBs. The identified pathophysiology of reward dysfunction may be useful to tailor future treatments.
Similar content being viewed by others
Data availability
Data available upon request.
References
Andersson, J. L. R., Jenkinson, M., & Smith, S. (2007). Non-linear optimisation. FMRIB technial report TR07JA1. University of Oxford FMRIB Centre.
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6(2), 115–116.
Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2014). Inhibition and the right inferior frontal cortex: One decade on. Trends in Cognitive Sciences, 18(4), 177–185. https://doi.org/10.1016/j.tics.2013.12.003
Arzeno Ferrao, Y., Almeida, V. P., Bedin, N. R., Rosa, R., & D’Arrigo, B. E. (2006). Impulsivity and compulsivity in patients with trichotillomania or skin picking compared with patients with obsessive-compulsive disorder. Comprehensive Psychiatry, 47(4), 282–288. https://doi.org/10.1016/j.comppsych.2005.11.005
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Series B, 57, 289–300.
Bjork, J. M., Momenan, R., Smith, A. R., & Hommer, D. W. (2008). Reduced posterior mesofrontal cortex activation by risky rewards in substance-dependent patients. Drug and Alcohol Dependence, 95(1–2), 1158.
Chamberlain, S. R., Menzies, L. A., Fineberg, N. A., Del Campo, N., Suckling, J., Craig, K., Müller, U., Robbins, T. W., Bullmore, E. T., & Sahakian, B. J. (2008). Grey matter abnormalities in trichotillomania: Morphometric magnetic resonance imaging study. British Journal of Psychiatry, 193(3), 216–221. https://doi.org/10.1192/bjp.bp.107.048314
Chamberlain, S. R., Hampshire, A., Menzies, L. A., Garyfallidis, E., Grant, J. E., Odlaug, B. L., Craig, K., Fineberg, N., & Sahakian, B. J. (2010). Reduced brain white matter integrity in trichotillomania: A diffusion tensor imaging study. Archives of General Psychiatry, 67(9), 965–971. https://doi.org/10.1001/archgenpsychiatry.2010.109
Chamberlain, S. R., Harries, M., Redden, S. A., Keuthen, N. J., Stein, D. J., Lochner, C., & Grant, J. E. (2018). Cortical thickness abnormalities in trichotillomania: International multi-site analysis. Brain Imaging and Behavior, 12(3), 823–828. https://doi.org/10.1007/s11682-017-9746-3
Chambers, C. D., Bellgrove, M. A., Gould, I. C., English, T., Garavan, H., McNaught, E., Kamke, M., & Mattingley, J. B. (2007). Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. Journal of Neurophysiology, 98(6), 3638–3647. https://doi.org/10.1152/jn.00685.2007
Deepmala, S. J., Kumar, N., Delhey, L., Berk, M., Dean, O., Spielholz, C., & Frye, R. (2015). Clinical trials of N-acetylcysteine in psychiatry and neurology: A systematic review. Neuroscience and Biobehavioral Reviews, 55, 294–321. https://doi.org/10.1016/j.neubiorev.2015.04.015
Figee, M., Vink, M., de Geus, F., Vulink, N., Veltman, D. J., Westenberg, H., & Denys, D. (2011). Dysfunctional reward circuitry in obsessive-compulsive disorder. Biological Psychiatry, 69(9), 867–874. https://doi.org/10.1016/j.biopsych.2010.12.003
Grachev, I. D. (1997). MRI-based morphometric topographic parcellation of human neocortex in trichotillomania. Psychiatry and Clinical Neurosciences, 51(5), 315–321. https://doi.org/10.1111/j.1440-1819.1997.tb03205.x
Grant, J. E., Odlaug, B. L., & Potenza, M. N. (2007). Addicted to hair pulling? How an alternate model of trichotillomania may improve treatment outcome. Harvard Review of Psychiatry, 15(2), 80–85. https://doi.org/10.1080/10673220701298407
Grant, J. E., Odlaug, B. L., Hampshire, A., Schreiber, L. R., & Chamberlain, S. R. (2013). White matter abnormalities in skin picking disorder: A diffusion tensor imaging study. Neuropsychopharmacology, 38(5), 763–769. https://doi.org/10.1038/npp.2012.241
Grant, J. E., Daws, R., Hampshire, A., & Chamberlain, S. R. (2018). An fMRI pilot study of cognitive flexibility in trichotillomania. Journal of Neuropsychiatry and Clinical Neurosciences, 30(4), 318–324. https://doi.org/10.1176/appi.neuropsych.18030038
Hampshire, A., Chamberlain, S. R., Monti, M. M., Duncan, J., & Owen, A. M. (2010). The role of the right inferior frontal gyrus: Inhibition and attentional control. NeuroImage, 50(3), 1313–1319. https://doi.org/10.1016/j.neuroimage.2009.12.109
Isobe, M., Redden, S. A., Keuthen, N. J., Stein, D. J., Lochner, C., Grant, J. E., & Chamberlain, S. R. (2018). Striatal abnormalities in trichotillomania: A multi-site MRI analysis. Neuroimage Clinical, 17, 893–898. https://doi.org/10.1016/j.nicl.2017.12.031
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. https://doi.org/10.1016/s1053-8119(02)91132-8
Jia, Z., Worhunsky, P. D., Carroll, K. M., Rounsaville, B. J., Stevens, M. C., Pearlson, G. D., & Potenza, M. N. (2011). An initial study of neural responses to monetary incentives as related to treatment outcome in cocaine dependence. Biological Psychiatry, 70(6), 553–560. https://doi.org/10.1016/j.biopsych.2011.05.008
Keuthen, N. J., Makris, N., Schlerf, J. E., Martis, B., Savage, C. R., McMullin, K., Seidman, L. J., Schmahmann, J. D., Kennedy, D. N., Hodge, S. M., & Rauch, S. L. (2007). Evidence for reduced cerebellar volumes in trichotillomania. Biological Psychiatry, 61(3), 374–381. https://doi.org/10.1016/j.biopsych.2006.06.013
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport, 12(17), 3683–3687. https://doi.org/10.1097/00001756-200112040-00016
Knutson, B., & Greer, S. M. (2008). Anticipatory affect: Neural correlates and consequences for choice. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1511), 3771–3786. https://doi.org/10.1098/rstb.2008.0155
Lee, J. A., Kim, C. K., Jahng, G. H., Hwang, L. K., Cho, Y. W., Kim, Y. J., Lee, W. H., Moon, S. J., Cho, A. R., & Bahn, G. H. (2010). A pilot study of brain activation in children with trichotillomania during a visual-tactile symptom provocation task: A functional magnetic resonance imaging study. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 34(7), 1250–1258. https://doi.org/10.1016/j.pnpbp.2010.06.031
Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 35(5), 1219–1236. https://doi.org/10.1016/j.neubiorev.2010.12.012
Odlaug, B. L., Chamberlain, S. R., Derbyshire, K. L., Leppink, E. W., & Grant, J. E. (2014). Impaired response inhibition and excess cortical thickness as candidate endophenotypes for trichotillomania. Journal of Psychiatric Research, 59, 167–173. https://doi.org/10.1016/j.jpsychires.2014.08.010
Odlaug, B. L., Hampshire, A., Chamberlain, S. R., & Grant, J. E. (2016). Abnormal brain activation in excoriation (skin-picking) disorder:Evidence from an executive planning fMRI study. British Journal of Psychiatry, 208(2), 168–174. https://doi.org/10.1192/bjp.bp.114.155192
O’Sullivan, R. L., Rauch, S. L., Breiter, H. C., Grachev, I. D., Baer, L., Kennedy, D. N., Keuthen, N. J., Savage, C. R., Manzo, P. A., Caviness, V. S., & Jenike, M. A. (1997). Reduced basal ganglia volumes in trichotillomania measured via morphometric magnetic resonance imaging. Biological Psychiatry, 42(1), 39–45. https://doi.org/10.1016/S0006-3223(96)00297-1
Rauch, S. L., Wright, C. I., Savage, C. R., Martis, B., McMullin, K. G., Wedig, M. M., Gold, A. L., & Keuthen, N. J. (2007). Brain activation during implicit sequence learning in individuals with trichotillomania. Psychiatry Research, 154(3), 233–240. https://doi.org/10.1016/j.pscychresns.2006.09.002
Roos, A., Grant, J. E., Fouche, J. P., Stein, D. J., & Lochner, C. (2015). A comparison of brain volume and cortical thickness in excoriation (skin picking) disorder and trichotillomania (hair pulling disorder) in women. Behavioural Brain Research, 279, 255–258. https://doi.org/10.1016/j.bbr.2014.11.029
Sani, G., Gualtieri, I., Paolini, M., Bonanni, L., Spinazzola, E., Maggiora, M., Pinzone, V., Brugnoli, R., Angeletti, G., Girardi, P., Rapinesi, C., & Kotzalidis, G. D. (2019). Drug treatment of trichotillomania (hair-pulling disorder), excoriation (skin-picking) disorder, and nail-biting (onychophagia). Current Neuropharmacology, 17(8), 775–786. https://doi.org/10.2174/1570159X17666190320164223
Schienle, A., Übel, S., & Wabnegger, A. (2018). Visual symptom provocation in skin picking disorder: An fMRI study. Brain Imaging and Behavior, 12(5), 1504–1512. https://doi.org/10.1007/s11682-017-9792-x
Schlosser, S., Black, D. W., Blum, N., & Goldstein, R. B. (1994). The demography, phenomenology, and family history of 22 persons with compulsive hair-pulling. Annals of Clinical Psychiatry, 6, 147–152.
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., & Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (MINI): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59, 22–57.
Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.
Stein, D. J., Coetzer, R., Lee, M., Davids, B., & Bouwer, C. (1997). Magnetic resonance brain imaging in women with obsessive-compulsive disorder and trichotillomania. Psychiatry Research, 74(3), 177–182. https://doi.org/10.1016/s0925-4927(97)00010-3
Swedo, S. E., Rapoport, J. L., Leonard, H. L., Schapiro, M. B., Rapoport, S. I., & Grady, C. L. (1991). Regional cerebral glucose metabolism of women with trichotillomania. Archives of General Psychiatry, 48(9), 828–833. https://doi.org/10.1001/archpsyc.1991.01810330052008
Tucker, B. T., Woods, D. W., Flessner, C. A., Franklin, S. A., & Franklin, M. E. (2011). The skin picking impact project: Phenomenology, interference, and treatment utilization of pathological skin picking in a population-based sample. Journal of Anxiety Disorders, 25(1), 88–95. https://doi.org/10.1016/j.janxdis.2010.08.007
Wabnegger, A., & Schienle, A. (2019). The role of the cerebellum in skin-picking disorder. Cerebellum, 18(1), 91–98. https://doi.org/10.1007/s12311-018-0957-y
White, M. P., Shirer, W. R., Molfino, M. J., Tenison, C., Damoiseaux, J. S., & Greicius, M. D. (2013). Disordered reward processing and functional connectivity in trichotillomania: A pilot study. Journal of Psychiatric Research, 47(9), 1264–1272. https://doi.org/10.1016/j.jpsychires.2013.05.014
Funding
This study was funded by the Body-Focused Precision Medicine Initiative Granted by The TLC Foundation for Body-Focused Repetitive Behaviors to University of Chicago (Dr. Grant), Massachusetts General Hospital (MGH)/Harvard (Dr. Keuthen), and University of California, Los Angeles (UCLA) (Dr. Piacentini). Dr. Chamberlain’s involvement in this study was funded by a Wellcome Trust Clinical Fellowship (Refs. 110049/Z/15/Z & 110049/Z/15/A). The TLC Foundation for Body-Focused Repetitive Behaviors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. This study was completed with support from the REDCap project at the University of Chicago, which is hosted and managed by the Center for Research Informatics and funded by the Biological Sciences Division and by the Institute for Translational Medicine, CTSA Grant Number UL1 TR000430 from the National Institutes of Health.
Author information
Authors and Affiliations
Contributions
JEG, TP, ER, SRC, JS, DD, DW, JP, NJK all made substantial contributions to the conception or design of the work as well as the acquisition, analysis, or interpretation of data; they all aided in drafting the work, gave final approval of the version to be published; and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Conflict of interest
Dr. Grant has received research grants from Biohaven, Promentis, and Otsuka Pharmaceuticals. Dr. Grant receives yearly compensation from Springer Publishing for acting as Editor-in-Chief of the Journal of Gambling Studies and has received royalties from Oxford University Press, American Psychiatric Publishing, Inc., Norton Press, and McGraw Hill. Dr. Chamberlain consults for Promentis; and receives stipends from Elsevier for editorial journal work. The other authors report no conflicts. Dr. Dougherty receives research support and honoraria from Medtronic, Inc. Dr. Woods has received royalties from Oxford University Press and Springer Press. Dr. Piacentini has received research grants from NIMH, the Tourette Association of America, and Pfizer. He receives travel support and honoraria from the Tourette Association of America and the International OCD Foundation and book royalties from Guilford Publications and Oxford University Press. Dr Keuthen has received prior research grants from The TLC Foundation for Body-Focused Repetitive Behaviors and royalties from New Harbinger, Inc. The remaining authors have nothing to disclose.
Ethical approval
The Institutional Review Boards for the University of Chicago, University of California, Los Angeles, and Massachusetts General Hospital/Harvard Medical School approved the study and the informed consent. Data sharing agreements were arranged across all sites and neuroimaging equipment was synced across the sites. The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008.
Informed consent
Prior to obtaining written informed consent, the investigators provided a complete description of the study, discussed potential risks, and answered questions regarding the study. After that, participants provided written informed consent.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Grant, J.E., Peris, T.S., Ricketts, E.J. et al. Reward processing in trichotillomania and skin picking disorder. Brain Imaging and Behavior 16, 547–556 (2022). https://doi.org/10.1007/s11682-021-00533-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-021-00533-5