Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-23T18:16:45.064Z Has data issue: false hasContentIssue false

Reward learning deficits in Parkinson's disease depend on depression

Published online by Cambridge University Press:  04 April 2017

M. H. M. Timmer*
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands Department of Neurology and Parkinson Center Nijmegen (ParC), Radboud University Medical Center, Nijmegen, The Netherlands
G. Sescousse
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands
M. E. van der Schaaf
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands
R. A. J. Esselink
Affiliation:
Department of Neurology and Parkinson Center Nijmegen (ParC), Radboud University Medical Center, Nijmegen, The Netherlands
R. Cools
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Medical Center, Nijmegen, The Netherlands
*
*Address for correspondence: M. H. M. Timmer, M.D., Department of Neurology (HP 935), Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands. (Email: Monique.Timmer@radboudumc.nl)

Abstract

Background

Depression is one of the most common and debilitating non-motor symptoms of Parkinson's disease (PD). The neurocognitive mechanisms underlying depression in PD are unclear and treatment is often suboptimal.

Methods

We investigated the role of striatal dopamine in reversal learning from reward and punishment by combining a controlled medication withdrawal procedure with functional magnetic resonance imaging in 22 non-depressed PD patients and 19 PD patients with past or present depression.

Results

PD patients with a depression (history) exhibited impaired reward v. punishment reversal learning as well as reduced reward v. punishment-related BOLD signal in the striatum (putamen) compared with non-depressed PD patients. No effects of dopaminergic medication were observed.

Conclusions

The present findings demonstrate that impairments in reversal learning from reward v. punishment and associated striatal signalling depend on the presence of (a history of) depression in PD.

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

Bodi, N, Keri, S, Nagy, H, Moustafa, A, Myers, CE, Daw, N, Dibo, G, Takats, A, Bereczki, D, Gluck, MA (2009). Reward-learning and the novelty-seeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinsons patients. Brain 132, 23852395.CrossRefGoogle Scholar
Clark, L, Chamberlain, SR, Sahakian, BJ (2009). Neurocognitive mechanisms in depression: implications for treatment. Annual Review of Neuroscience 32, 5774.Google Scholar
Cools, R, Altamirano, L, D'esposito, M (2006). Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 44, 16631673.Google Scholar
Cools, R, Frank, MJ, Gibbs, SE, Miyakawa, A, Jagust, W, D'esposito, M (2009). Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. Journal of Neuroscience 29, 15381543.Google Scholar
Cools, R, Robinson, OJ, Sahakian, B (2008). Acute tryptophan depletion in healthy volunteers enhances punishment prediction but does not affect reward prediction. Neuropsychopharmacology 33, 22912299.Google Scholar
Der-Avakian, A, Markou, A (2012). The neurobiology of anhedonia and other reward-related deficits. Trends in Neurosciences 35, 6877.Google Scholar
Epstein, J, Pan, H, Kocsis, JH, Yang, YH, Butler, T, Chusid, J, Hochberg, H, Murrough, J, Strohmayer, E, Stern, E, Silbersweig, DA (2006). Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. American Journal of Psychiatry 163, 17841790.CrossRefGoogle ScholarPubMed
Eshel, N, Roiser, JP (2010). Reward and punishment processing in depression. Biological Psychiatry 68, 118124.CrossRefGoogle ScholarPubMed
Esselink, RAJ, De Bie, RMA, De Haan, RJ, Lenders, M, Nijssen, PCG, Staal, MJ, Smeding, HMM, Schuurman, PR, Bosch, DA, Speelman, JD (2004). Unilateral pallidotomy versus bilateral subthalamic nucleus stimulation in PD – a randomized trial. Neurology 62, 201207.CrossRefGoogle ScholarPubMed
Folstein, Mf, Folstein, SE, Mchugh, PR (1975). Mini-mental state – practical method for grading cognitive state of patients for clinician. Journal of Psychiatric Research 12, 189198.Google Scholar
Forbes, EE, Hariri, AR, Martin, SL, Silk, JS, Moyles, DL, Fisher, PM, Brown, SM, Ryan, ND, Birmaher, B, Axelson, DA, Dahl, RE (2009). Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. American Journal of Psychiatry 166, 6473.Google Scholar
Forbes, EE, Shaw, DS, Dahl, RE (2007). Alterations in reward-related decision making in boys with recent and future depression. Biological Psychiatry 61, 633639.Google Scholar
Frank, MJ, Seeberger, LC, O'reilly, RC (2004). By carrot or by stick: cognitive reinforcement learning in Parkinsonism. Science 306, 19401943.CrossRefGoogle ScholarPubMed
Goetz, CG, Stebbins, GT (2004). Assuring interrater reliability for the UPDRS motor section: utility of the UPDRS teaching tape. Movement Disorders 19, 14531456.CrossRefGoogle ScholarPubMed
Helmich, RC, Janssen, MJR, Oyen, WJG, Bloem, BR, Toni, I (2011). Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson tremor. Annals of Neurology 69, 269281.Google Scholar
Henriques, JB, Glowacki, JM, Davidson, RJ (1994). Reward fails to alter response bias in depression. Journal of Abnormal Psychology 103, 460466.Google Scholar
Howell, DC (1997). Statistical Methods for Psychology. Wadsworth Publishing Company: Belmont, USA.Google Scholar
Ishihara, L, Brayne, C (2006). A systematic review of depression and mental illness preceding Parkinson's disease. Acta Neurologica Scandinavica 113, 211220.Google Scholar
Janssen, LK, Sescousse, G, Hashemi, MM, Timmer, MH, Ter Huurne, NP, GEURTS, DE, COOLS, R (2015). Abnormal modulation of reward versus punishment learning by a dopamine D2-receptor antagonist in pathological gamblers. Psychopharmacology (Berl) 232, 33453353.Google Scholar
Kobza, S, Ferrea, S, Schnitzler, A, Pollok, B, Sudmeyer, M, Bellebaum, C (2012). Dissociation between active and observational learning from positive and negative feedback in Parkinsonism. PLoS ONE 7, e5025050258.Google Scholar
Maia, TV, Frank, MJ (2011). From reinforcement learning models to psychiatric and neurological disorders. Nature Neuroscience 14, 154162.Google Scholar
Moustafa, AA, Cohen, MX, Sherman, SJ, Frank, MJ (2008). A role for dopamine in temporal decision making and reward maximization in Parkinsonism. Journal of Neuroscience 28, 1229412304.CrossRefGoogle ScholarPubMed
Murphy, FC, Michael, A, Robbins, TW, Sahakian, BJ (2003). Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychological Medicine 33, 455467.CrossRefGoogle ScholarPubMed
Palminteri, S, Lebreton, M, Worbe, Y, Grabli, D, Hartmann, A, Pessiglione, M (2009). Pharmacological modulation of subliminal learning in Parkinson's and Tourette's syndromes. Proceedings of the National Academy of Sciences of the United States of America 106, 1917919184.Google Scholar
Pizzagalli, DA, Holmes, AJ, Dillon, DG, Goetz, EL, Birk, JL, Bogdan, R, Dougherty, DD, Iosifescu, DV, Rauch, SL, Fava, M (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. American Journal of Psychiatry 166, 702710.CrossRefGoogle ScholarPubMed
Pizzagalli, DA, Jahn, AL, O'shea, JP (2005). Toward an objective characterization of an anhedonic phenotype: a signal detection approach. Biological Psychiatry 57, 319327.CrossRefGoogle ScholarPubMed
Poser, BA, Versluis, MJ, Hoogduin, JM, Norris, DG (2006). BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: parallel-acquired inhomogeneity-desensitized fMRI. Magnetic Resonance in Medicine 55, 12271235.Google Scholar
Reijnders, J, Ehrt, U, Weber, WEJ, Aarsland, D, Leentjens, AFG (2008). A systematic review of prevalence studies of depression in Parkinson's disease. Movement Disorders 23, 183189.Google Scholar
Remy, P, Doder, M, Lees, A, Turjanski, N, Brooks, D (2005). Depression in Parkinson's disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128, 13141322.CrossRefGoogle ScholarPubMed
Robinson, MD, Moeller, SK, Fetterman, AK (2010 a). Neuroticism and responsiveness to error feedback: adaptive self-regulation versus affective reactivity. Journal of Personality 78, 14691496.Google Scholar
Robinson, OJ, Cools, R, Carlisi, CO, Sahakian, BJ, Drevets, WC (2011). Ventral striatum response during reward and punishment reversal learning in unmedicated major depressive disorder. American Journal of Psychiatry 169, 152159.Google Scholar
Robinson, OJ, Cools, R, Sahakian, BJ (2012). Tryptophan depletion disinhibits punishment but not reward prediction: implications for resilience. Psychopharmacology 219, 599605.Google Scholar
Robinson, OJ, Frank, MJ, Sahakian, BJ, Cools, R (2010 b). Dissociable responses to punishment in distinct striatal regions during reversal learning. Neuroimage 51, 14591467.CrossRefGoogle ScholarPubMed
Roiser, JP, Elliott, R, Sahakian, BJ (2012). Cognitive mechanisms of treatment in depression. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 37, 117136.Google Scholar
Rutledge, RB, Lazzaro, SC, Lau, B, Myers, CE, Gluck, MA, Glimcher, PW (2009). Dopaminergic drugs modulate learning rates and perseveration in Parkinson's patients in a dynamic foraging task. Journal of Neuroscience 29, 1510415114.Google Scholar
Schmand, B, Bakker, D, Saan, R, Louman, J (1991). The Dutch reading test for adults: a measure of premorbid intelligence level. Tijdschrift Voor Gerontologie en Geriatrie 22, 1519.Google Scholar
Schultz, W, Dickinson, A (2000). Neuronal coding of prediction errors. Annual Review of Neuroscience 23, 473500.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (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, 2233.Google ScholarPubMed
Shiba, M, Bower, JH, Maraganore, DM, McDonnell, SK, Peterson, BJ, Ahlskog, JE, Schaid, DJ, Rocca, WA (2000). Anxiety disorders and depressive disorders preceding Parkinson's disease: A case-control study. Movement Disorders 15, 669677.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Smittenaar, P, Chase, HW, Aarts, E, Nusselein, B, Bloem, BR, Cools, R (2012). Decomposing effects of dopaminergic medication in Parkinson's disease on probabilistic action selection – learning or performance? European Journal of Neuroscience 35, 11441151.Google Scholar
Steele, JD, Kumar, P, Ebmeier, KP (2007). Blunted response to feedback information in depressive illness. Brain 130, 23672374.Google Scholar
Taylor Tavares, JV, Clark, L, Furey, ML, Williams, GB, Sahakian, BJ, Drevets, WC (2008). Neural basis of abnormal response to negative feedback in unmedicated mood disorders. Neuroimage 42, 11181126.Google Scholar
Thirion, B, Pinel, P, Meriaux, S, Roche, A, Dehaene, S, Poline, JB (2007). Analysis of a large fMRI cohort: statistical and methodological issues for group analyses. Neuroimage 35, 105120.CrossRefGoogle ScholarPubMed
Treadway, MT, Zald, DH (2013). Parsing anhedonia: translational models of reward-processing deficits in psychopathology. Current Directions in Psychological Science 22, 244249.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273289.Google Scholar
Van Der Schaaf, ME, Van Schouwenburg, MR, Geurts, DE, Schellekens, AF, Buitelaar, JK, Verkes, RJ, Cools, R (2014). Establishing the dopamine dependency of human striatal signals during reward and punishment reversal learning. Cerebral Cortex 24, 633642.CrossRefGoogle ScholarPubMed
Vriend, C, Raijmakers, P, VeltmaN, DJ, Van Dijk, KD, Van Der Werf, YD, Foncke, EM, Smit, JH, Berendse, HW, Van Den Heuvel, OA (2013). Depressive symptoms in Parkinson's disease are related to reduced [123I]FP-CIT binding in the caudate nucleus. Journal of Neurology Neurosurgery and Psychiatry 85, 159164.Google Scholar
Weintraub, D, Newberg, AB, Cary, MS, Siderowf, AD, Moberg, PJ, Kleiner-Fisman, G, Duda, JE, Stern, MB, Mozley, D, Katz, IR (2005). Striatal dopamine transporter imaging correlates with anxiety and depression symptoms in Parkinson's disease. Journal of Nuclear Medicine 46, 227232.Google Scholar
Whitton, AE, Treadway, MT, Pizzagalli, DA (2015). Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Current Opinion in Psychiatry 28, 712.Google Scholar
Supplementary material: File

Timmer supplementary material

Timmer supplementary material 1

Download Timmer supplementary material(File)
File 940.6 KB