Experimental Brain Research

, Volume 208, Issue 1, pp 1–10 | Cite as

Impaired conflict monitoring in Parkinson’s disease patients during an oculomotor redirect task

  • Ausaf A. Farooqui
  • Neha Bhutani
  • Shrikanth Kulashekhar
  • Madhuri Behari
  • Vinay Goel
  • Aditya Murthy
Research Article


Fallibility is inherent in human cognition and so a system that will monitor performance is indispensable. While behavioral evidence for such a system derives from the finding that subjects slow down after trials that are likely to produce errors, the neural and behavioral characterization that enables such control is incomplete. Here, we report a specific role for dopamine/basal ganglia in response conflict by accessing deficits in performance monitoring in patients with Parkinson’s disease. To characterize such a deficit, we used a modification of the oculomotor countermanding task to show that slowing down of responses that generate robust response conflict, and not post-error per se, is deficient in Parkinson’s disease patients. Poor performance adjustment could be either due to impaired ability to slow RT subsequent to conflicts or due to impaired response conflict recognition. If the latter hypothesis was true, then PD subjects should show evidence of impaired error detection/correction, which was found to be the case. These results make a strong case for impaired performance monitoring in Parkinson’s patients.


Conflicts Error correction Saccades Basal ganglia Double-step Countermanding 


  1. Angel RW (1971) L-dopa and error correction time in Parkinson’s disease. Neurology 21:1255–1260PubMedGoogle Scholar
  2. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Pschyol Rev 108:624–652CrossRefGoogle Scholar
  3. Boucher L, Palmeri TJ, Logan GD, Schall JD (2007) Inhibitory control in mind and brain an interactive race model of countermanding saccades. Psychol Rev 114:376–397PubMedCrossRefGoogle Scholar
  4. Bradley VA, Welch JL, Dick DJ (1989) Visuospatial working memory in Parkinson’s disease. J Neurol Neurosurg Psychiatry 52:1228–1235PubMedCrossRefGoogle Scholar
  5. Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson’s disease. Exp Brain Res 129:38–48PubMedCrossRefGoogle Scholar
  6. Camalier CR, Gotlier A, Murthy A, Thompson KG, Logan GD, Palmeri TJ, Schall JD (2007) Dynamics of saccade target selection: race model analysis of double-step saccade and search-step saccade production in human and macaque. Vis Res 47:2187–2211PubMedCrossRefGoogle Scholar
  7. Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP (2005) Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 43:784–796PubMedCrossRefGoogle Scholar
  8. Dehaene S, Posner MI, Tucker DM (1994) Localisation of a neural system for error detection and compensation. Psychol Sci 5:303–305CrossRefGoogle Scholar
  9. Dehaene S, Kerzberg M, Changeux JP (1998) A neuronal model of a global workspace in effortful cognitive tasks. PNAS 95:14529–14534PubMedCrossRefGoogle Scholar
  10. Divac I, Rosvild HE, Szwarcbart MK (1967) Behavioral effects of selective ablation of caudate nucles. J Comp Physiol Psychol 63:184–190PubMedCrossRefGoogle Scholar
  11. Dum RP, Strick PL (1993) Cingulate motor areas. In: Vogt BA, Gabriel M (eds) Neurobiology of cingulate cortex and limbic thalamus, 1st edn. Birkhäuser, Boston, pp 415–441Google Scholar
  12. Emeric EE, Brown JW, Carpenter RH, Hanes DP, Harris R, Logan GD, Mashru RN, Pare M, Pouget P, Stuphorn V, Taylor TL, Schall JD (2007) Influence of history on saccade countermanding performance in humans and macaque monkeys. Vis Res 47:35–49PubMedCrossRefGoogle Scholar
  13. Falkenstein M, Hielscher H, Dziobek I, Schwarzenau P, Hoormann J, Sunderman B, Hohnsbein J (2001) Action monitoring, error detection and the basal ganglia: An ERP study. Neuro Report 12:157–161Google Scholar
  14. Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E (1993) A neural system for error detection and compensation. Psychol Sci 4:385–390CrossRefGoogle Scholar
  15. Hanes DP, Patterson WF II, Schall JD (1998) Role of frontal eye fields in countermanding saccades: visual, movement and fixation activity. J Neurophysiol 79:817–834PubMedGoogle Scholar
  16. Hatanaka N, Tokuno H, Hamada I, Inase M, Ito Y, Imanishi M, Hasegawa N, Akazawa T, Nambu A, Takada M (2003) Thalamocortical and intracortical connections of monkey cingulate motor areas. J Comp Neurol 462:121–138PubMedCrossRefGoogle Scholar
  17. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedGoogle Scholar
  18. Holroyd CB, Coles MG (2002) The neural basis of human error processing: reinforcement learning, dopamine and error-related negativity. Psychol Rev 109:679–709PubMedCrossRefGoogle Scholar
  19. Holroyd CB, Praamstra P, Plat E, Coles MG (2002) Spared error-related potentials in mild to moderate parkinson’s disease. Neuropsychologia 40:2116–2124PubMedCrossRefGoogle Scholar
  20. Ito J, Kitagawa J (2006) Performance monitoring and error processing during a lexical decision task in patients with Parkinson’s disease. J Geriatr Psychiatry Neurol 19:46–54PubMedCrossRefGoogle Scholar
  21. Joti P, Kulashekhar S, Behari M, Murthy A (2007) Impaired inhibitory control in patients with Parkinson’s disease. Exp Brain Res 177:447–457PubMedCrossRefGoogle Scholar
  22. Kapoor V, Murthy A (2008) Covert inhibition potentiates online control in a double-step task. J Vis 8:1–16PubMedCrossRefGoogle Scholar
  23. Kingstone A, Klein R, Morein-Zamir S, Hunt A, Fisk J, Maxner C (2002) Orienting attention in aging and Parkinson’s disease: distinguishing models of control. J Clin Exp Neuropsychol 24:951–967PubMedCrossRefGoogle Scholar
  24. Lewis SZ, Slabosz A, Robbins TW, Barker RA, Owen AM (2005) Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson’s disease. Neuropsychologia 43:823–832PubMedCrossRefGoogle Scholar
  25. Lo CC, Wang XJ (2006) Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat Neurosci 9:953–963CrossRefGoogle Scholar
  26. Logan GD (1985) Executive control of thought and action. Acta Psychol 60:193–210CrossRefGoogle Scholar
  27. Murthy A, Ray S, Shorter SM, Schall JD, Thompson KG (2009) Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. J Neurophysiol 101:2485–2507PubMedCrossRefGoogle Scholar
  28. Ottes FP, Van Gisbergen JA, Eggermont JJ (1984) Metrics of saccade responses to visual double stimuli: two different modes. Vis Res 24:1169–1179PubMedCrossRefGoogle Scholar
  29. Owen AM (2004) Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry. Neuroscientist 10:525–537PubMedCrossRefGoogle Scholar
  30. Rabbitt PMA (1966) Errors and error-correction in choice response tasks. J Exp Psychol 71:264–272PubMedCrossRefGoogle Scholar
  31. Rabbitt PMA (1968) Three kinds of error signaling responses in serial choice task. Q J Exp Psychol 20:179–188PubMedCrossRefGoogle Scholar
  32. Ramakrishnan A, Chokandre S, Murthy A (2010) Voluntary control of multi-gaze shifts during movement preparation and execution. J Neurophysiol 103:2400–2416PubMedCrossRefGoogle Scholar
  33. Redgrave K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neurosci 89:1009–1023CrossRefGoogle Scholar
  34. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306:443–447PubMedCrossRefGoogle Scholar
  35. Roll A, Wierzbicka M, Wolf W (1996) The ‘gap paradigm’ leads to express-like saccadic reaction times in Parkinson’s disease. Exp Brain Res 111:131–138PubMedCrossRefGoogle Scholar
  36. Schall JD (2001) Neural basis of deciding, choosing and acting. Nat Rev Neurosci 2:33–42PubMedCrossRefGoogle Scholar
  37. Schultz W (1997) A neural substrate of prediction and reward. Science 14:1593–1599CrossRefGoogle Scholar
  38. Schultz W, Romo R (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp Brain Res 91:363–384PubMedCrossRefGoogle Scholar
  39. Shallice T (1988) From neuropsychology to mental structure. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  40. Shallice T, Burgess P (1996) The domain of supervisory processes and temporal organization of behaviour. Philos Trans R Soc Lond B Biol Sci 351:1405–1411PubMedCrossRefGoogle Scholar
  41. Stemmer B, Segalowitz SJ, Dywan J, Panisset M, Melmed C (2007) The error negativity in medicated and non-medicated patients with Parkinson’s Disease. Clin Neurophysiol 118:1223–1229PubMedCrossRefGoogle Scholar
  42. Stuphorn V, Schall JD (2002) Neuronal control and monitoring of initiation of movements. Muscle Nerve 26:326–339PubMedCrossRefGoogle Scholar
  43. Stuss DT, Benson DF (1986) The frontal lobes. Raven Press, New YorkGoogle Scholar
  44. Swick D, Turken AU (2002) Dissociation between conflict detection and error monitoring in the human anterior cingulated cortex. Proc Natl Acad Sci USA 99:16354–16359PubMedCrossRefGoogle Scholar
  45. Ullsperger M, von Cramon DY (2004) Subprocesses of performance monitoring: a dissociation of error processing and response competition revealed by event-related fMRI and ERPs. Neuroimage 14:1387–1401CrossRefGoogle Scholar
  46. Willemssen R, Muller T, Schwarz M, Falkenstein M, Beste C (2009) Response monitoring in de novo patients with Parkinson’s disease. Plos One 4:e4898PubMedCrossRefGoogle Scholar
  47. Williams ZM, Bush G, Rauch SL, Cosgrove GR, Eskander EN (2004) Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat Neurosci 7:1370–1375PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ausaf A. Farooqui
    • 1
    • 2
  • Neha Bhutani
    • 1
  • Shrikanth Kulashekhar
    • 1
    • 3
  • Madhuri Behari
    • 4
  • Vinay Goel
    • 4
  • Aditya Murthy
    • 1
    • 5
  1. 1.National Brain Research CentreManesarIndia
  2. 2.MRC Cognition and Brain Science UnitCambridgeUK
  3. 3.Neuroscience Centre, University of HelsinkiHelsinkiFinland, UK
  4. 4.Department of NeurologyCN Centre, All India Institute of Medical SciencesNew DelhiIndia
  5. 5.Centre for Neuroscience, Indian Institute of ScienceBangaloreIndia

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