Journal of Neural Transmission

, Volume 122, Issue 5, pp 653–660 | Cite as

Impaired cognitive control in Parkinson’s disease patients with freezing of gait in response to cognitive load

  • Courtney C. Walton
  • James M. Shine
  • Loren Mowszowski
  • Moran Gilat
  • Julie M. Hall
  • Claire O’Callaghan
  • Sharon L. Naismith
  • Simon J. G. Lewis
Neurology and Preclinical Neurological Studies - Original Article

Abstract

Freezing of gait is a frequent and disabling symptom experienced by many patients with Parkinson’s disease. A number of executive deficits have been shown to be associated with the phenomenon suggesting a common underlying pathophysiology, which as of yet remains unclear. Neuroimaging studies have also implicated the role of the cognitive control network in patients with freezing. To explore this concept, the current study examined error-monitoring as a measure of cognitive control. Thirty-four patients with and 38 without freezing of gait, who were otherwise well matched on disease severity, completed a colour-word interference task that allowed the specific assessment of error monitoring during conflict. Whilst both groups performed colour-naming and word-reading tasks equally well, those patients with freezing showed a pattern between conditions whereby they were better able to monitor performance and self-correct errors in the pure inhibition task but not after a switching rule was introduced. The novel results shown here provide insight into possible pathophysiological mechanisms involved in cognitive load and error monitoring in patients with freezing of gait. These results provide further evidence for the role of functional frontostriatal circuitry impairments in patients with freezing of gait and have implications for future studies and possible therapeutic interventions.

Keywords

Freezing of gait Parkinson’s disease Executive function Error monitoring Stroop task Cognitive control 

References

  1. Alegre M et al (2013) The subthalamic nucleus is involved in successful inhibition in the stop-signal task: a local field potential study in Parkinson’s disease. Exp Neurol 239:1–12. doi:10.1016/j.expneurol.2012.08.027 CrossRefPubMedGoogle Scholar
  2. Amboni M, Cozzolino A, Longo K, Picillo M, Barone P (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23:395–400. doi:10.1002/mds.21850 CrossRefPubMedGoogle Scholar
  3. Amboni M, Barone P, Picillo M, Cozzolino A, Longo K, Erro R, Iavarone A (2010) A two-year follow-up study of executive dysfunctions in parkinsonian patients with freezing of gait at on-state. Mov Disord 25:800–802. doi:10.1002/mds.23033 CrossRefPubMedGoogle Scholar
  4. Amboni M, Barone P, Hausdorff JM (2013) Cognitive contributions to gait and falls: evidence and implications. Mov Disord 28:1520–1533. doi:10.1002/mds.25674 CrossRefPubMedCentralPubMedGoogle Scholar
  5. Aron AR, Poldrack RA (2006) Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26:2424–2433. doi:10.1523/JNEUROSCI.4682-05.2006 CrossRefPubMedGoogle Scholar
  6. Aron AR, Robbins TW, Poldrack RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Neurosci 18(4):177–185. doi:10.1016/j.tics.2013.12.003 CrossRefGoogle Scholar
  7. Beck A, Steer R, Brown G (1996) Manual for the BDI-II. Psychological Corporation, San AntonioGoogle Scholar
  8. Brittain JS et al (2012) A role for the subthalamic nucleus in response inhibition during conflict. J Neurosci 32:13396–13401. doi:10.1523/JNEUROSCI.2259-12.2012 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Brown JW (2013) Beyond conflict monitoring: cognitive control and the neural basis of thinking before you act. Curr Dir Psychol Sci 22:179–185. doi:10.1177/0963721412470685 CrossRefPubMedCentralPubMedGoogle Scholar
  10. Brown RG, Marsden CD (1988) Internal versus external cues and the control of attention in Parkinson’s disease brain. J Neurol 111(Pt 2):323–345Google Scholar
  11. Cohen RG et al (2014) Inhibition, executive function, and freezing of gait. J Parkinson’s Dis 4:111–122. doi:10.3233/JPD-130221 Google Scholar
  12. Crawford JR, Sutherland D, Garthwaite PH (2008) On the reliability and standard errors of measurement of contrast measures from the D-KEFS. J Int Neuropsychol 14:1069–1073. doi:10.1017/S1355617708081228 CrossRefGoogle Scholar
  13. Delis DC, Kaplan E, Kramer JH (2001) Delis-Kaplan executive function system (D-KEFS). Psychological Corporation, San Antonio, TX Google Scholar
  14. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20–24. doi:10.1001/archneur.64.1.20 CrossRefPubMedGoogle Scholar
  15. Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  16. Frank MJ (2006) Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw 19:1120–1136. doi:10.1016/j.neunet.2006.03.006 CrossRefPubMedGoogle Scholar
  17. Garavan H, Ross TJ, Kaufman J, Stein EA (2003) A midline dissociation between error-processing and response-conflict monitoring. Neuroimage 20:1132–1139. doi:10.1016/S1053-8119(03)00334-3 CrossRefPubMedGoogle Scholar
  18. Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD (2000) Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord 6:165–170CrossRefPubMedGoogle Scholar
  19. Giladi N et al (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm 108:53–61CrossRefPubMedGoogle Scholar
  20. Goetz CG et al (2008) Movement Disorder Society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170. doi:10.1002/mds.22340 CrossRefPubMedGoogle Scholar
  21. Gray P, Hildebrand K (2000) Fall risk factors in Parkinson’s disease. J Neurosci Nurs 32:222–228CrossRefPubMedGoogle Scholar
  22. Hall JM, Shine JM, Walton CC, Gilat M, Kamsma YP, Naismith SL, Lewis SJ (2014) Early phenotypic differences between Parkinson’s disease patients with and without freezing of gait. Parkinsonism Relat Disord. doi:10.1016/j.parkreldis.2014.02.028 PubMedCentralGoogle Scholar
  23. Haynes WI, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for Basal Ganglia models and deep brain stimulation. J Neurosci 33:4804–4814. doi:10.1523/JNEUROSCI.4674.12.2013 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Heremans E et al (2013a) Cognitive aspects of freezing of gait in Parkinson’s disease: a challenge for rehabilitation. J Neur Transm 120:543–557. doi:10.1007/s00702-012-0964-y CrossRefGoogle Scholar
  25. Heremans E, Nieuwboer A, Vercruysse S (2013b) Freezing of gait in Parkinson’s disease: where are we now? Curr Neurol Neurosci Rep 13:350. doi:10.1007/s11910-013-0350-7 CrossRefPubMedGoogle Scholar
  26. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442CrossRefPubMedGoogle Scholar
  27. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184CrossRefPubMedCentralPubMedGoogle Scholar
  28. Klein TA, Endrass T, Kathmann N, Neumann J, von Cramon DY, Ullsperger M (2007) Neural correlates of error awareness. Neuroimage 34:1774–1781. doi:10.1016/j.neuroimage.2006.11.014 CrossRefPubMedGoogle Scholar
  29. Kornblum S, Hasbroucq T, Osman A (1990) Dimensional overlap: cognitive basis for stimulus-response compatibility—a model and taxonomy. Psychol Rev 97:253–270CrossRefPubMedGoogle Scholar
  30. Lewis SJ, Barker RA (2009) A pathophysiological model of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 15:333–338. doi:10.1016/j.parkreldis.2008.08.006 CrossRefPubMedGoogle Scholar
  31. Matar E, Shine JM, Naismith SL, Lewis SJ (2013) Using virtual reality to explore the role of conflict resolution and environmental salience in Freezing of Gait in Parkinson’s disease. Parkinsonism Relat Disord. doi:10.1016/j.parkreldis.2013.06.002 PubMedGoogle Scholar
  32. Mirelman A, Maidan I, Deutsch JE (2013) Virtual reality and motor imagery: promising tools for assessment and therapy in Parkinson’s disease. Mov Disord 28:1597–1608. doi:10.1002/mds.25670 CrossRefPubMedGoogle Scholar
  33. Moore O, Peretz C, Giladi N (2007) Freezing of gait affects quality of life of peoples with Parkinson’s disease beyond its relationships with mobility and gait. Mov Disord 22:2192–2195. doi:10.1002/mds.21659 CrossRefPubMedGoogle Scholar
  34. Naismith SL, Shine JM, Lewis SJ (2010) The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord 25:1000–1004. doi:10.1002/mds.23005 CrossRefPubMedGoogle Scholar
  35. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–117CrossRefPubMedGoogle Scholar
  36. Narayanan NS, Cavanagh JF, Frank MJ, Laubach M (2013) Common medial frontal mechanisms of adaptive control in humans and rodents. Nat Neurosci 16:1888–1895. doi:10.1038/nn.3549 CrossRefPubMedGoogle Scholar
  37. Nelson H, Willison J (1991) The revised national adult reading test–test manual Windsor: NFER-NelsonGoogle Scholar
  38. Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS (2012) Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 12:241–268. doi:10.3758/s13415-011-0083-5 CrossRefPubMedCentralPubMedGoogle Scholar
  39. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744. doi:10.1016/S1474-4422(11)70143-0 CrossRefPubMedGoogle Scholar
  40. Obeso I et al (2014) The subthalamic nucleus and inhibitory control: impact of subthalamotomy in Parkinson’s disease. Brain 137:1470–1480. doi:10.1093/brain/awu058 CrossRefPubMedGoogle Scholar
  41. Orr C, Hester R (2012) Error-related anterior cingulate cortex activity and the prediction of conscious error awareness. Front Hum Neurosci 6:177. doi:10.3389/fnhum.2012.00177 CrossRefPubMedCentralPubMedGoogle Scholar
  42. Pieruccini-Faria F, Jones JA, Almeida QJ (2014) Motor planning in Parkinson’s disease patients experiencing freezing of gait: the influence of cognitive load when approaching obstacles. Brain Cogn 87:76–85. doi:10.1016/j.bandc.2014.03.005 CrossRefPubMedGoogle Scholar
  43. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306:443–447. doi:10.1126/science.1100301 CrossRefPubMedGoogle Scholar
  44. Sharp DJ, Bonnelle V, De Boissezon X, Beckmann CF, James SG, Patel MC, Mehta MA (2010) Distinct frontal systems for response inhibition, attentional capture, and error processing. Proc Natl Acad Sci USA 107:6106–6111. doi:10.1073/pnas.1000175107 CrossRefPubMedCentralPubMedGoogle Scholar
  45. Shine JM et al (2013a) Exploring the cortical and subcortical functional magnetic resonance imaging changes associated with freezing in Parkinson’s disease. Brain 136:1204–1215. doi:10.1093/brain/awt049 CrossRefPubMedGoogle Scholar
  46. Shine JM, Matar E, Ward PB, Bolitho SJ, Pearson M, Naismith SL, Lewis SJ (2013b) Differential neural activation patterns in patients with Parkinson’s disease and freezing of gait in response to concurrent cognitive and motor load. PloS One 8:e52602. doi:10.1371/journal.pone.0052602 CrossRefPubMedCentralPubMedGoogle Scholar
  47. Shine JM et al (2013c) Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain 136:3671–3681. doi:10.1093/brain/awt272 CrossRefPubMedGoogle Scholar
  48. Shine JM, Moustafa AA, Matar E, Frank MJ, Lewis SJ (2013d) The role of frontostriatal impairment in freezing of gait in Parkinson’s disease Frontiers in Systems Neuroscience 7 doi:10.3389/fnsys.2013.00061
  49. Shine JM, Naismith SL, Palavra NC, Lewis SJ, Moore ST, Dilda V, Morris TR (2013e) Attentional set-shifting deficits correlate with the severity of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 19:388–390. doi:10.1016/j.parkreldis.2012.07.015 CrossRefPubMedGoogle Scholar
  50. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653. doi:10.1002/mds.23429 CrossRefPubMedGoogle Scholar
  51. Vandenbossche J, Deroost N, Soetens E, Spildooren J, Vercruysse S, Nieuwboer A, Kerckhofs E (2011) Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabil Neural Repair 25:765–773. doi:10.1177/1545968311403493 CrossRefPubMedGoogle Scholar
  52. Vandenbossche J et al (2012) Conflict and freezing of gait in Parkinson’s disease: support for a response control deficit. Neuroscience 206:144–154. doi:10.1016/j.neuroscience.2011.12.048 CrossRefPubMedGoogle Scholar
  53. Vandenbossche J et al (2013a) Freezing of gait in Parkinson’s disease: disturbances in automaticity and control. Front Hum Neurosci 6:356. doi:10.3389/fnhum.2012.00356 CrossRefPubMedCentralPubMedGoogle Scholar
  54. Vandenbossche J et al (2013b) Impaired implicit sequence learning in Parkinson’s disease patients with freezing of gait. Neuropsychology 27:28–36. doi:10.1037/a0031278 CrossRefPubMedGoogle Scholar
  55. Wager TD, Jonides J, Reading S (2004) Neuroimaging studies of shifting attention: a meta-analysis. NeuroImage 22:1679–1693. doi:10.1016/j.neuroimage.2004.03.052 CrossRefPubMedGoogle Scholar
  56. Walton CC, Shine JM, Mowszowski L, Naismith SL, Lewis SJ (2014) Freezing of gait in Parkinson’s disease: current treatments and the potential role for cognitive training. Restor Neurology Neurosci 32:411–422. doi:10.3233/rnn-130370 Google Scholar
  57. Wessel JR (2012) Error awareness and the error-related negativity: evaluating the first decade of evidence. Front Hum Neurosci 6:88. doi:10.3389/fnhum.2012.00088 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Courtney C. Walton
    • 1
    • 2
  • James M. Shine
    • 1
  • Loren Mowszowski
    • 1
    • 2
  • Moran Gilat
    • 1
  • Julie M. Hall
    • 1
  • Claire O’Callaghan
    • 3
  • Sharon L. Naismith
    • 1
    • 2
  • Simon J. G. Lewis
    • 1
  1. 1.Parkinson’s Disease Research Clinic, Brain and Mind Research InstituteUniversity of SydneySydneyAustralia
  2. 2.Healthy Brain Ageing Program, Brain and Mind Research InstituteUniversity of SydneySydneyAustralia
  3. 3.Neuroscience Research Australia and School of Medical SciencesUniversity of New South WalesSydneyAustralia

Personalised recommendations