Mapping anticipatory anhedonia: an fMRI study

Springer Science and Business Media LLC - Tập 13 - Trang 1624-1634 - 2019
Joanna E. Szczepanik1,2, Jessica L. Reed1, Allison C. Nugent1, Elizabeth D. Ballard1, Jennifer W. Evans1, Carl W. Lejuez3, Carlos A. Zarate1
1Section on the Neurobiology and Treatment of Mood Disorders, Intramural Research Program, National Institute of Mental Health, National Institutes of Health, Bethesda, USA
2Division of Translational Research, Extramural Research Program, National Institute of Mental Health, National Institutes of Health, Bethesda, USA
3Department of Psychology, University of Kansas, Lawrence, USA

Tóm tắt

Anhedonia—broadly defined as loss of interest and/or an inability to experience pleasure—is an important feature of several psychiatric disorders. Research into the clinical presentation and neurobiology of this symptom has identified components related to motivation, learning, anticipation, and experience of pleasure as important constructs that inform therapeutic interventions. The experimental study of anhedonia is largely based on incentive processing paradigms, most often with monetary rewards, though studies have also used pleasantness ratings of various stimuli. However, linking an individual’s own system of reinforcers and ability to enjoy them with anhedonia and neural activity remains comparatively under-explored. A previous study of participants with major depressive disorder (MDD) and healthy controls found that activity word ratings correlated with measures of anhedonia, depression, and motivation. The present study collected functional magnetic resonance imaging (fMRI) images in healthy controls while they rated activity words and pictures showing activities in order to identify networks differentially responsive to subjective decisions about the appetitive value of activities. The study sought to measure individually-relevant hedonic capacity as demonstrated by correlations between task measures and anticipatory anhedonia ratings. Ratings of potential pleasure were associated with neural activity in areas previously identified as relevant to pleasure and reward processing, such as anterior and posterior cingulate, middle frontal areas, and dorsal and ventral striatum. Although the study included only healthy controls, the results demonstrate a link between anhedonia measures, behavior, and brain responses and also test a paradigm that could be used to study anhedonia in clinical populations.

Tài liệu tham khảo

Aharon, I., Etcoff, N., Ariely, D., Chabris, C. F., O’Connor, E., & Breiter, H. C. (2001). Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron, 32, 537–551.

Arrondo, G., Murray, G. K., Hill, E., Szalma, B., Yathiraj, K., Denman, C., & Dudas, R. B. (2015). Hedonic and disgust taste perception in borderline personality disorder and depression. British Journal of Psychiatry, 207, 79–80.

Beck, A. T., & Beamesderfer, A. (1974). Assessment of depression: the depression inventory. Modern Problems of Pharmacopsychiatry, 7, 151–169.

Berridge, K. C., & Kringelbach, M. L. (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berlin), 199(3), 457–480.

Chen, G., Saad, Z. S., Britton, J. C., Pine, D. S., & Cox, R. W. (2013). Linear mixed-effects modeling approach to FMRI group analysis. NeuroImage, 73(Supplement C), 176–190.

Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.

Craske, M. G., Meuret, A. E., Ritz, T., Treanor, M., & Dour, H. J. (2016). Treatment for anhedonia: a neuroscience driven approach. Depression and Anxiety, 33(10), 927–938.

Dichter, G. S., Smoski, M. J., Kampov-Polevoy, A. B., Gallop, R., & Garbutt, J. C. (2010). Unipolar depression does not moderate responses to the sweet taste test. Depression and Anxiety, 27(9), 859–863.

Dowd, E. C., & Barch, D. M. (2012). Pavlovian reward prediction and receipt in schizophrenia: relationship to anhedonia. PLoS One, 7(5), e35622.

Eickhoff, S. B., Laird, A. R., Grefkes, C., Wang, L. E., Zilles, K., & Fox, P. T. (2009). Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping, 30(9), 2907–2926.

First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. (2002). Structured clinical interview for DSM-IV-TR Axis I disorders, research version, non-patient edition (SCID-I/NP). New York, NY: Biometrics Research, New York State Psychiatric Institute.

Frey, A.-L., Malinowska, L., Harley, K., Salhi, L., Iqbal, S., Sharma, S., & McCabe, C. (2015). Investigating subtypes of reward processing deficits as trait markers for depression. Translational Developmental Psychiatry, 3(1), 27517.

Gard, D. E., Gard, M. G., Kring, A. M., & John, O. P. (2006). Anticipatory and consummatory components of the experience of pleasure: a scale development study. Journal of Research in Personality, 40(6), 1086–1102.

Groenewold, N. A., Opmeer, E. M., de Jonge, P., Aleman, A., & Costafreda, S. G. (2013). Emotional valence modulates brain functional abnormalities in depression: evidence from a meta-analysis of fMRI studies. Neuroscience & Biobehavioral Reviews, 37, 152–163.

Heller, A. S., Johnstone, T., Shackman, A. J., Light, S. N., Peterson, M. J., Kolden, G. G., Kalin, N. H., & Davidson, R. J. (2009). Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proceedings of the National Academy of Sciences of the United States of America, 106, 22445–22450.

Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., Sanislow, C., & Wang, P. (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry, 167(7), 748–751.

Jenkins, L. M., Skerrett, K. A., DelDonno, S. R., Patron, V. G., Meyers, K. K., Peltier, S., et al. (2018). Individuals with more severe depression fail to sustain nucleus accumbens activity to preferred music over time. Psychiatry Research: Neuroimaging, 275, 21–27.

Keedwell, P. A., Andrew, C., Williams, S. C. R., Brammer, M. J., & Phillips, M. L. (2005). The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry, 58(11), 843–853.

Keller, J., Young, C. B., Kelley, E., Prater, K., Levitin, D. J., & Menon, V. (2013). Trait anhedonia is associated with reduced reactivity and connectivity of mesolimbic and paralimbic reward pathways. Journal of Psychiatric Research, 47(10), 1319–1328.

Kiefer, M., & Pulvermuller, F. (2012). Conceptual representations in mind and brain: theoretical developments, current evidence and future directions. Cortex, 48, 805–825.

Kuhn, S., & Gallinat, J. (2012). The neural correlates of subjective pleasantness. Neuroimage, 61(1), 289–294.

Lally, N., Nugent, A. C., Luckenbaugh, D. A., Ameli, R., Roiser, J. P., & Zarate, C. A. (2014). Anti-anhedonic effect of ketamine and its neural correlates in treatment-resistant bipolar depression. Translational Psychiatry, 4, e469.

Lally, N., Nugent, A. C., Luckenbaugh, D. A., Niciu, M. J., Roiser, J. P., & Zarate, C. A., Jr. (2015). Neural correlates of change in major depressive disorder anhedonia following open-label ketamine. Journal of Psychopharmacology, 29(5), 596–607.

McCabe, C. (2016). Neural signals of ‘intensity’ but not ‘wanting’ or ‘liking’ of rewards may be trait markers for depression. Journal of Psychopharmacology, 30, 1020–1027.

McMakin, D. L., Olino, T. M., Porta, G., Dietz, L. J., Emslie, G., Clarke, G., Wagner, K. D., Asarnow, J. R., Ryan, N. D., Birmaher, B., Shamseddeen, W., Mayes, T., Kennard, B., Spirito, A., Keller, M., Lynch, F. L., Dickerson, J. F., & Brent, D. A. (2012). Anhedonia predicts poorer recovery among youth with selective serotonin reuptake inhibitor treatment–resistant depression. Journal of the American Academy of Child & Adolescent Psychiatry, 51(4), 404–411.

Mrochen, A., Marxreiter, F., Kohl, Z., Schlachetzki, J., Renner, B., Schenk, T., Winkler, J., & Klucken, J. (2016). From sweet to sweat: hedonic olfactory range is impaired in Parkinson’s disease. Parkinsonism & Related Disorders, 22, 9–14.

Pizzagalli, D. A. (2011). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology, 36, 183–206.

Pizzagalli, D. A., Holmes, A. J., Dillon, D. G., Goetz, E. L., Birk, J. L., Bogdan, R., et al. (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. American Journal of Psychiatry, 166, 702–710.

Rizvi, S. J., Pizzagalli, D. A., Sproule, B. A., & Kennedy, S. H. (2016). Assessing anhedonia in depression: potentials and pitfalls. Neuroscience & Biobehavioral Reviews, 65, 21–35.

Rømer Thomsen, K., Whybrow, P. C., & Kringelbach, M. L. (2015). Reconceptualizing anhedonia: novel perspectives on balancing the pleasure networks in the human brain. Frontiers in Behavioral Neuroscience, 9, 49.

Schultz, W. (2001). Reward signaling by dopamine neurons. Neuroscientist, 7(4), 293–302.

Sherdell, L., Waugh, C., & Gotlib, I. (2012). Anticipatory pleasure predicts motivation for reward in major depression. Journal of Abnormal Psychology, 121(1), 51–60.

Smoski, M. J., Felder, J., Bizzell, J., Green, S. R., Ernst, M., Lynch, T. R., & Dichter, G. S. (2009). fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. Journal of Affective Disorders, 118(1–3), 69–78.

Snaith, R. P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., & Trigwell, P. (1995). A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. British Journal of Psychiatry, 167(1), 99–103.

Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the state-trait anxiety inventory. Palo Alto: Consulting Psychologists Press.

Szczepanik, J. E., Furey, M. L., Nugent, A. C., Henter, I. D., Zarate, C. A., Jr., & Lejuez, C. W. (2017). Altered interaction with environmental reinforcers in major depressive disorder: relationship to anhedonia. Behaviour Research and Therapy, 97, 170–177.

Talairach, J., & Tournoux, P. (1988). Co‐planar stereotaxic atlas of the human brain: 3‐D proportional system: an approach to cerebral imaging. New York: Georg Thieme.

Tamir, M., & Robinson, M. D. (2007). The happy spotlight: positive mood and selective attention to rewarding information. Personality and Social Psychology Bulletin, 33(8), 1124–1136.

Taube, W., Mouthon, M., Leukel, C., Hoogewoud, H.-M., Annoni, J.-M., & Keller, M. (2015). Brain activity during observation and motor imagery of different balance tasks: an fMRI study. Cortex, 64(Supplement C, 102–114.

Treadway, M. T., & Zald, D. H. (2011). Reconsidering anhedonia in depression: lessons from translational neuroscience. Neuroscience & Biobehavioral Reviews, 35(3), 537–555.

Ubl, B., Kuehner, C., Kirsch, P., Ruttorf, M., Diener, C., & Flor, H. (2015). Altered neural reward and loss processing and prediction error signalling in depression. Social Cognitive and Affective Neuroscience, 10(8), 1102–1112.

Uher, R., Perlis, R. H., Henigsberg, N., Zobel, A., Rietschel, M., Mors, O., Hauser, J., Dernovsek, M. Z., Souery, D., Bajs, M., Maier, W., Aitchison, K. J., Farmer, A., & McGuffin, P. (2012). Depression symptom dimensions as predictors of antidepressant treatment outcome: replicable evidence for interest-activity symptoms. Psychological Medicine, 42(05), 967–980.

Vessel, E. A., Starr, G. G., & Rubin, N. (2012). The brain on art: intense aesthetic experience activates the default mode network. Frontiers in Human Neuroscience, 6, 66.

Vrieze, E., Demyttenaere, K., Bruffaerts, R., Hermans, D., Pizzagalli, D. A., Sienaert, P., Hompes, T., de Boer, P., Schmidt, M., & Claes, S. (2014). Dimensions in major depressive disorder and their relevance for treatment outcome. Journal of Affective Disorders, 155(0), 35–41.

Yin, H., Tully, L. M., Lincoln, S. H., & Hooker, C. I. (2015). Adults with high social anhedonia have altered neural connectivity with ventral lateral prefrontal cortex when processing positive social signals. Frontiers in Human Neuroscience, 9, 469.

Young, C. B., Chen, T., Nusslock, R., Keller, J., Schatzberg, A. F., & Menon, V. (2016). Anhedonia and general distress show dissociable ventromedial prefrontal cortex connectivity in major depressive disorder. Translational Psychiatry, 6(5), e810.

Zhang, W.-N., Chang, S.-H., Guo, L.-Y., Zhang, K.-L., & Wang, J. (2013). The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. Journal of Affective Disorders, 151(2), 531–539.

Zhang, B., Lin, P., Shi, H., Ongur, D., Auerbach, R. P., Wang, X., et al. (2016). Mapping anhedonia-specific dysfunction in a transdiagnostic approach: an ALE meta-analysis. Brain Imaging and Behavior, 10(3), 920–939.

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