Skip to main content
Log in

Neural correlates of emotional valence processing in Parkinson’s disease: dysfunction in the subcortex

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Parkinson’s disease (PD) is frequently accompanied by cognitive and neuropsychiatric symptoms including impairments in affective processing. Despite this, mechanisms underlying vulnerability to deficits in affective processing remain unclear. In this study, we utilized functional Magnetic Resonance Imaging (fMRI) and an Affective Go-NoGo paradigm, to examine the neural correlates of emotional valence processing in PD. Results suggest that PD is associated with aberrant processing of emotional valence in subcortical limbic structures. Specifically, we found significant group-by-valence interactions in the ventral striatum and amygdala in response to words of differing emotional valence. Our findings contribute to a broader understanding of affective processing in PD and may provide insights into the mechanisms underlying vulnerability to mood disorders in PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AGNG:

Affective Go-NoGo

PD:

Parkinson’s disease

VTA:

Ventral Tegmental Area

References

  • Arsalidou, M., Duerden, E. G., & Taylor, M. J. (2013). The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia. Human Brain Mapping, 34(11), 3031–3054.

    Article  Google Scholar 

  • Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38(1), 95–113.

    Article  Google Scholar 

  • Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck depression inventory-II psychological corporation. TX: San Antonio.

    Google Scholar 

  • Bell, P. T., Gilat, M., O'Callaghan, C., Copland, D. A., Frank, M. J., Lewis, S. J., et al. (2015). Dopaminergic basis for impairments in functional connectivity across subdivisions of the striatum in Parkinson's disease. Human Brain Mapping, 36(4), 1278–1291.

    Article  Google Scholar 

  • Bertrand, E., Lechowicz, W., Lewandowska, E., Szpak, G. M., Dymecki, J., Kosno-Kruszewska, E., et al. (2003). Degenerative axonal changes in the hippocampus and amygdala in Parkinson's disease. Folia Neuropathologica, 41(4), 197–207.

    PubMed  Google Scholar 

  • Bianciardi M, Toschi N, Eichner C, Polimeni JR, Setsompop K, Brown EN, et al. In vivo functional connectome of human brainstem nuclei of the ascending arousal, autonomic, and motor systems by high spatial resolution 7-Tesla fMRI. Magma (New York, NY) 2016; 29(3): 451–62.

  • Bond, A., & Lader, M. (1974). The use of analogue scales in rating subjective feelings. British Journal of Medical Psychology, 47(3), 211–218.

    Article  Google Scholar 

  • Bowers, D., Miller, K., Mikos, A., Kirsch-Darrow, L., Springer, U., Fernandez, H., et al. (2006). Startling facts about emotion in Parkinson's disease: Blunted reactivity to aversive stimuli. Brain, 129(Pt 12), 3356–3365.

    Article  Google Scholar 

  • Braak, H., Braak, E., Yilmazer, D., de Vos, R. A., Jansen, E. N., Bohl, J., et al. (1994). Amygdala pathology in Parkinson's disease. Acta Neuropathologica, 88(6), 493–500.

    Article  CAS  Google Scholar 

  • Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N., & Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiology of Aging, 24(2), 197–211.

    Article  Google Scholar 

  • Bradley M, Lang P. Affective norms for English words (ANEW): Instruction manual and affective ratings. NIMH Center for Emotion and Attention University of Florida 1999.

  • Brett, Matthew, et al. (2002) "Region of interest analysis using the MarsBar toolbox for SPM 99." Neuroimage 16.2 S497.

  • Bright, P., Jaldow, E., & Kopelman, M. D. (2002). The National Adult Reading Test as a measure of premorbid intelligence: A comparison with estimates derived from demographic variables. Journal of the International Neuropsychological Society, 8(6), 847–854.

    Article  Google Scholar 

  • Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010). Dopamine in motivational control: Rewarding, aversive, and alerting. Neuron, 68(5), 815–834.

    Article  CAS  Google Scholar 

  • Brown, P. (2007). Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Current Opinion in Neurobiology, 17(6), 656–664.

    Article  CAS  Google Scholar 

  • Bruck, A., Aalto, S., Nurmi, E., Vahlberg, T., Bergman, J., & Rinne, J. O. (2006). Striatal subregional 6-[18F]fluoro-L-dopa uptake in early Parkinson's disease: A two-year follow-up study. Movement Disorders : Official Journal of the Movement Disorder Society, 21(7), 958–963.

    Article  Google Scholar 

  • Chan, S. W., Goodwin, G. M., & Harmer, C. J. (2007). Highly neurotic never-depressed students have negative biases in information processing. Psychological Medicine, 37(9), 1281–1291.

    Article  Google Scholar 

  • Chaudhuri, K. R., & Schapira, A. H. (2009). Non-motor symptoms of Parkinson's disease: Dopaminergic pathophysiology and treatment. Lancet Neurology, 8(5), 464–474.

    Article  CAS  Google Scholar 

  • Dalrymple-Alford, J. C., MacAskill, M. R., Nakas, C. T., Livingston, L., Graham, C., Crucian, G. P., et al. (2010). The MoCA: Well-suited screen for cognitive impairment in Parkinson disease. Neurology, 75(19), 1717–1725.

    Article  CAS  Google Scholar 

  • Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Shehzad, Z., et al. (2008). Functional connectivity of human striatum: a resting state FMRI study. Cerebral cortex (New York, NY: 1991) 18(12), 2735–47.

  • Drevets, W. C., Price, J. L., & Furey, M. L. (2008). Brain structural and functional abnormalities in mood disorders: Implications for neurocircuitry models of depression. Brain Structure & Function, 213(1–2), 93–118.

    Article  Google Scholar 

  • Dubbelink, K. T., Stoffers, D., Deijen, J. B., Twisk, J. W., Stam, C. J., Hillebrand, A., et al. (2013). Resting-state functional connectivity as a marker of disease progression in Parkinson's disease: A longitudinal MEG study. NeuroImage Clinical, 2, 612–619.

    Article  Google Scholar 

  • Elliott, R., Ogilvie, A., Rubinsztein, J. S., Calderon, G., Dolan, R. J., & Sahakian, B. J. (2004). Abnormal ventral frontal response during performance of an affective go/no go task in patients with mania. Biological Psychiatry, 55(12), 1163–1170.

    Article  Google Scholar 

  • Elliott, R., Rubinsztein, J. S., Sahakian, B. J., & Dolan, R. J. (2000). Selective attention to emotional stimuli in a verbal go/no-go task: An fMRI study. Neuroreport, 11(8), 1739–1744.

    Article  CAS  Google Scholar 

  • Elliott, R., Rubinsztein, J. S., Sahakian, B. J., & Dolan, R. J. (2002a). The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry, 59(7), 597–604.

    Article  Google Scholar 

  • Elliott, R., Rubinsztein, J. S., Sahakian, B. J., & Dolan, R. J. (2002b). The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry, 59(7), 597–604.

    Article  Google Scholar 

  • Epstein, J., Pan, H., Kocsis, J. H., Yang, Y., Butler, T., Chusid, J., et al. (2006). Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. The American Journal of Psychiatry, 163(10), 1784–1790.

    Article  Google Scholar 

  • Erickson, K., Drevets, W. C., Clark, L., Cannon, D. M., Bain, E. E., Zarate Jr., C. A., et al. (2005). Mood-congruent bias in affective go/no-go performance of unmedicated patients with major depressive disorder. The American Journal of Psychiatry, 162(11), 2171–2173.

    Article  Google Scholar 

  • Fornito, A., Zalesky, A., & Breakspear, M. (2015). The connectomics of brain disorders. Nature Reviews Neuroscience, 16(3), 159–172.

    Article  CAS  Google Scholar 

  • Forstmann, B. U., de Hollander, G., van Maanen, L., Alkemade, A., & Keuken, M. C. (2016). Towards a mechanistic understanding of the human subcortex. Nature Reviews Neuroscience, 18(1), 57–65.

    Article  Google Scholar 

  • Freire, L., Roche, A., & Mangin, J. F. (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging, 21(5), 470–484.

    Article  CAS  Google Scholar 

  • Goetz, C. G., Fahn, S., Martinez-Martin, P., Poewe, W., Sampaio, C., Stebbins, G. T., et al. (2007). Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): Process, format, and clinimetric testing plan. Movement disorders: official journal of the Movement Disorder Society 22(1), 41–7.

  • Golden, S. A., Christoffel, D. J., Heshmati, M., Hodes, G. E., Magida, J., Davis, K., et al. (2013). Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nature Medicine, 19(3), 337–344.

    Article  CAS  Google Scholar 

  • Gopin, C. B., Burdick, K. E., Derosse, P., Goldberg, T. E., & Malhotra, A. K. (2011). Emotional modulation of response inhibition in stable patients with bipolar I disorder: A comparison with healthy and schizophrenia subjects. Bipolar Disorders, 13(2), 164–172.

    Article  Google Scholar 

  • Gray, H. M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson's disease. Neuropsychology, 24(2), 176–191.

    Article  Google Scholar 

  • Haas, B. W., Omura, K., Constable, R. T., & Canli, T. (2007). Emotional conflict and neuroticism: Personality-dependent activation in the amygdala and subgenual anterior cingulate. Behavioral Neuroscience, 121(2), 249–256.

    Article  Google Scholar 

  • Hacker, C. D., Perlmutter, J. S., Criswell, S. R., Ances, B. M., & Snyder, A. Z. (2012). Resting state functional connectivity of the striatum in Parkinson's disease. Brain : A Journal of Neurology, 135(Pt 12), 3699–3711.

    Article  Google Scholar 

  • Hanganu A, Bedetti C, Degroot C, Mejia-Constain B, Lafontaine A-L, Soland V, et al. Mild cognitive impairment is linked with faster rate of cortical thinning in patients with Parkinson’s disease longitudinally; 2014.

  • Harding, A. J., Stimson, E., Henderson, J. M., & Halliday, G. M. (2002). Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. Brain, 125(Pt 11), 2431–2445.

    Article  Google Scholar 

  • Hayward, G., Goodwin, G. M., Cowen, P. J., & Harmer, C. J. (2005). Low-dose tryptophan depletion in recovered depressed patients induces changes in cognitive processing without depressive symptoms. Biological Psychiatry, 57(5), 517–524.

    Article  CAS  Google Scholar 

  • Hillier, A., Beversdorf, D. Q., Raymer, A. M., Williamson, D. J., & Heilman, K. M. (2007). Abnormal emotional word ratings in Parkinson's disease. Neurocase, 13(2), 81–85.

    Article  CAS  Google Scholar 

  • Hosokai, Y., Nishio, Y., Hirayama, K., Takeda, A., Ishioka, T., Sawada, Y., et al. (2009). Distinct patterns of regional cerebral glucose metabolism in Parkinson's disease with and without mild cognitive impairment. Movement Disorders : Official Journal of the Movement Disorder Society, 24(6), 854–862.

    Article  Google Scholar 

  • Hu, X., et al. (2015). Abnormal functional connectivity of the amygdala is associated with depression in Parkinson's disease. Mov Disord. 2015 Feb; 30(2), 238–44. doi:10.1002/mds.26087. Epub 2014 Dec 27.

  • Kilford EJ, Foulkes L, Potter R, Collishaw S, Thapar A, Rice F. Affective bias and current, past and future adolescent depression: A familial high risk study. Journal of Affective Disorders 2015; 174(0), 265–271.

  • Kousta, S.-T., Vinson, D. P., Vigliocco G. (2009). Emotion words, regardless of polarity, have a processing advantage over neutral words. Cognition, 112, 473–481. doi:10.1016/j.cognition.2009.06.007.

  • Korgaonkar, M. S., Fornito, A., Williams, L. M., & Grieve, S. M. (2014). Abnormal structural networks characterize major depressive disorder: A connectome analysis. Biological Psychiatry, 76(7), 567–574.

    Article  Google Scholar 

  • Kwak, Y., Peltier, S., Bohnen, N. I., Muller, M. L., Dayalu, P., & Seidler, R. D. (2010). Altered resting state cortico-striatal connectivity in mild to moderate stage Parkinson's disease. Frontiers in Systems Neuroscience, 4, 143.

    Article  CAS  Google Scholar 

  • LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184.

    Article  CAS  Google Scholar 

  • Mavridis, I., Boviatsis, E., & Anagnostopoulou, S. (2011). The human nucleus accumbens suffers parkinsonism-related shrinkage: A novel finding. Surgical and Radiologic Anatomy, 33(7), 595–599.

    Article  Google Scholar 

  • Mobes, J., Joppich, G., Stiebritz, F., Dengler, R., & Schroder, C. (2008). Emotional speech in Parkinson's disease. Movement disorders : Official Journal of the Movement Disorder Society, 23(6), 824–829.

    Article  Google Scholar 

  • Moore RY. Organization of midbrain dopamine systems and the pathophysiology of Parkinson's disease. Parkinsonism Relat Disord 2003; 9, Supplement 2: 65–71.

  • Murphy, F. C., Sahakian, B. J., Rubinsztein, J. S., Michael, A., Rogers, R. D., Robbins, T. W., et al. (1999). Emotional bias and inhibitory control processes in mania and depression. Psychological Medicine, 29(6), 1307–1321.

    Article  CAS  Google Scholar 

  • O'Callaghan, C., Naismith, S. L., Hodges, J. R., Lewis, S. J. G., & Hornberger, M. (2013). Fronto-striatal atrophy correlates of inhibitory dysfunction in Parkinson's disease versus behavioural variant frontotemporal dementia. Cortex, 49(7), 1833–1843.

    Article  Google Scholar 

  • Ochsner, K. N., & Gross, J. J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9(5), 242–249.

    Article  Google Scholar 

  • Ouchi, Y., Yoshikawa, E., Okada, H., Futatsubashi, M., Sekine, Y., Iyo, M., et al. (1999). Alterations in binding site density of dopamine transporter in the striatum, orbitofrontal cortex, and amygdala in early Parkinson's disease: Compartment analysis for beta-CFT binding with positron emission tomography. Annals of Neurology, 45(5), 601–610.

    Article  CAS  Google Scholar 

  • Peron, J., Dondaine, T., Le Jeune, F., Grandjean, D., & Verin, M. (2012). Emotional processing in Parkinson's disease: A systematic review. Movement disorders : official journal of the Movement Disorder Society, 27(2), 186–199.

    Article  Google Scholar 

  • Phillips, M., Drevets, W., Rauch, S., & Lane, R. (2003). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry, 54(5), 515–528.

    Article  Google Scholar 

  • 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. The American Journal of Psychiatry, 166(6), 702–710.

    Article  Google Scholar 

  • Postuma, R. B., & Dagher, A. (2006). Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cerebral Cortex, 16(10), 1508–1521.

    Article  Google Scholar 

  • Prodoehl, J., Yu, H., Little, D. M., Abraham, I., Vaillancourt, D. E. (2008). Region of interest template for the human basal ganglia: comparing EPI and standardized space approaches. NeuroImage 39(3), 956–65.

  • 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(Pt 6), 1314–1322.

    Article  Google Scholar 

  • Rhodes, R. A., Murthy, N. V., Dresner, M. A., Selvaraj, S., Stavrakakis N, Babar S, et al. (2007). Human 5-HT transporter availability predicts amygdala reactivity in vivo. The Journal of neuroscience: the official journal of the Society for Neuroscience 27(34), 9233–7.

  • Robinson, O. J., Cools, R., Carlisi, C. O., Sahakian, B. J., & Drevets, W. C. (2012). Ventral striatum response during reward and punishment reversal learning in unmedicated major depressive disorder. The American Journal of Psychiatry, 169(2), 152–159.

    Article  Google Scholar 

  • Roiser, J. P., Levy, J., Fromm, S. J., Goldman, D., Hodgkinson, C. A., Hasler, G., et al. (2012). Serotonin transporter genotype differentially modulates neural responses to emotional words following tryptophan depletion in patients recovered from depression and healthy volunteers. Journal of psychopharmacology (Oxford, England, 26(11), 1434–1442.

    Article  Google Scholar 

  • Roiser, J. P., Levy, J., Fromm, S. J., Nugent, A. C., Talagala, S. L., Hasler, G., et al. (2009). The effects of tryptophan depletion on neural responses to emotional words in remitted depression. Biological Psychiatry, 66(5), 441–450.

    Article  CAS  Google Scholar 

  • Roiser, J. P., Levy, J., Fromm, S. J., Wang, H., Hasler, G., Sahakian, B. J., et al. (2008). The effect of acute tryptophan depletion on the neural correlates of emotional processing in healthy volunteers. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 33(8), 1992–2006.

    Article  CAS  Google Scholar 

  • Russo, S. J., & Nestler, E. J. (2013). The brain reward circuitry in mood disorders. Nature Reviews Neuroscience, 14(10), 736.

    Article  CAS  Google Scholar 

  • Scatton, B., Rouquier, L., Javoy-Agid, F., & Agid, Y. (1982). Dopamine deficiency in the cerebral cortex in Parkinson disease. Neurology, 32(9), 1039–1040.

    Article  CAS  Google Scholar 

  • Sesack, S. R., & Grace, A. A. (2010). Cortico-basal ganglia reward network: Microcircuitry. Neuropsychopharmacology, 35(1), 27–47.

    Article  Google Scholar 

  • Shine, J. M., Matar, E., Ward, P. B., Bolitho, S. J., Gilat, M., Pearson, M., et al. (2013). Exploring the cortical and subcortical functional magnetic resonance imaging changes associated with freezing in Parkinson's disease. Brain: a journal of neurology 136(Pt 4), 1204–15.

  • Sieger, T., Serranová, T., Růžička, F., Vostatek, P., Wild, J., Šťastná, D., et al. (2015). Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus. Proceedings of the National Academy of Sciences, 112(10), 3116–3121.

    Article  CAS  Google Scholar 

  • Simons, G., Pasqualini, M. C., Reddy, V., & Wood, J. (2004). Emotional and nonemotional facial expressions in people with Parkinson's disease. Journal of the International Neuropsychological Society, 10(4), 521–535.

    Article  Google Scholar 

  • Spielberger CD, Gorssuch, R.L., Lushene, P.R., Vagg, P.R., & Jacobs, G.A Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press, Inc 1983.

  • Sporns, O. (2013). Structure and function of complex brain networks. Dialogues in Clinical Neuroscience, 15(3), 247–262.

    PubMed  PubMed Central  Google Scholar 

  • Starkstein, S. E., Mayberg, H. S., Preziosi, T. J., Andrezejewski, P., Leiguarda, R., & Robinson, R. G. (1992). Reliability, validity, and clinical correlates of apathy in Parkinson's disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 4(2), 134–139.

    Article  CAS  Google Scholar 

  • Swanson, L. W., Petrovich, G. D. (1998), What is the amygdala? Trends in neurosciences 21(8), 323–31.

  • Tang, Y., Ge, J., Liu, F., Wu, P., Guo, S., Liu, Z., et al. (2016). Cerebral metabolic differences associated with cognitive impairment in Parkinson's disease. PloS One, 11(4), e0152716.

    Article  Google Scholar 

  • Tard, C., Demailly, F., Delval, A., Semah, F., Defebvre, L., Dujardin, K., et al. (2015). Hypometabolism in posterior and temporal areas of the brain is associated with cognitive decline in Parkinson's disease. Journal of Parkinson's Disease, 5(3), 569–574.

    Article  Google Scholar 

  • Tessitore, A., Hariri, A. R., Fera, F., Smith, W. G., Chase, T. N., Hyde, T. M., et al. (2002). Dopamine modulates the response of the human amygdala: A study in Parkinson's disease. The Journal of Neuroscience, 22(20), 9099–9103.

    Article  CAS  Google Scholar 

  • Tomlinson, C. L., Stowe, R., Patel, S., Rick, C., Gray, R., & Clarke, C. E. (2010). Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Movement Disorders, 25(15), 2649–2653.

    Article  Google Scholar 

  • Visser, M., Leentjens, A. F., Marinus, J., Stiggelbout, A. M., & van Hilten, J. J. (2006). Reliability and validity of the Beck depression inventory in patients with Parkinson's disease. Movement disorders : Official Journal of the Movement Disorder Society, 21(5), 668–672.

    Article  Google Scholar 

  • Weintraub, D., Hoops, S., Shea, J. A., Lyons, K. E., Pahwa, R., Driver-Dunckley, E. D., et al. (2009). Validation of the questionnaire for impulsive-compulsive disorders in Parkinson's disease. Movement Disorders, 24(10), 1461–1467.

    Article  Google Scholar 

  • Wieser, M. J., Muhlberger, A., Alpers, G. W., Macht, M., Ellgring, H., & Pauli, P. (2006). Emotion processing in Parkinson's disease: Dissociation between early neuronal processing and explicit ratings. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 117(1), 94–102.

    Article  Google Scholar 

  • Yang, W., Liu, B., Huang, B., Huang, R., Wang, L., Zhang, Y., et al. (2016). Altered resting-state functional connectivity of the striatum in Parkinson's disease after levodopa administration. PloS One, 11(9), e0161935.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Samuel J. Bolitho for assistance with data collection and Dr. Claire O’Callaghan for critical appraisal on prior versions of the manuscript. Finally, we would like to thank all of the participants and their families for their involvement in this research.

Author contributions

PTB, KLM, DAC conceptualized the study; PTB, JMS, SJGL, DAC collected the data; PTB, MG, KLM, DAC analyzed the data; PTB wrote the initial draft; PTB, MG, JMS, KLM, SJGL edited the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter T. Bell.

Ethics declarations

Funding

Funded by Australian Research Council Future Fellowship FT100100976 to DAC.

Conflicts of interest

PTB, MG, JMS, KM, SJGL, DAC declare that they have no conflict of interest.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

Electronic supplementary material

ESM 1

(DOCX 23.7 kb)

Supplementary Figure 1

(JPEG 144 kb)

Supplementary Figure 2

(JPEG 119 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bell, P.T., Gilat, M., Shine, J.M. et al. Neural correlates of emotional valence processing in Parkinson’s disease: dysfunction in the subcortex. Brain Imaging and Behavior 13, 189–199 (2019). https://doi.org/10.1007/s11682-017-9754-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-017-9754-3

Keywords

Navigation