Skip to main content

Advertisement

SpringerLink
Log in

Dysfunctional action control as a specific feature of Parkinson’s disease

  • Neurology and Preclinical Neurological Studies - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

Parkinson’s disease (PD) is characterised by motor deficits as well as cognitive alterations, particularly concerning frontal lobe control. Here, we were interested in whether executive function is abnormal already early in PD, as well as whether this dysfunction worsens as a part of the dementia in PD. The following groups engaged in tasks addressing action control: PD patients with mild and advanced motor symptoms (aPD) without dementia, PD patients with dementia (PDD), patients with Alzheimer’s disease (AD) and healthy subjects (CON). Subjects either had to perform or inhibit button presses upon go and no-go cues, respectively. These cues were preceded by pre-cues, either randomly instructive of right or left hand preparation (switch condition), or repetitively instructive for one side only (non-switch condition). PDD and aPD omitted more go responses than CON. Furthermore, PDD disproportionally committed failures upon no-go cues compared to CON. In the non-switch condition, PDD performed worse than AD, whose deficits increased to the level of PDD in the switch condition. Over all PD patients, task performance correlated with disease severity. Under the switch condition, task performance was low in both PDD and AD. In the non-switch condition, this also held true for advanced PD patients (with and without dementia), but not for AD. Thus, the deficits evident in PDD appear to develop from imbalanced inhibitory-to-excitatory action control generally inherent to PD. These results specify the concept of dysexecution in PD and differentiate the cognitive profile of PDD from that of AD patients.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381. doi:10.1146/annurev.ne.09.030186.002041

    Article  CAS  PubMed  Google Scholar 

  • 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(3):395–400. doi:10.1002/mds.21850

    Article  PubMed  Google Scholar 

  • 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(6):800–802. doi:10.1002/mds.23033

    Article  PubMed  Google Scholar 

  • Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69(12):e55–e68. doi:10.1016/j.biopsych.2010.07.024

    Article  PubMed Central  PubMed  Google Scholar 

  • Baddeley A, Della Sala S (1996) Working memory and executive control. Philos Trans R Soc Lond Ser B Biol Sci 351(1346):1397–1403. doi:10.1098/rstb.1996.0123 (discussion 1403–1394)

    Article  CAS  Google Scholar 

  • Baddeley A, Logie R, Bressi S, Della Sala S, Spinnler H (1986) Dementia and working memory. Q J Exp Psychol A Hum Exp Psychol 38(4):603–618

    Article  CAS  Google Scholar 

  • Baddeley AD, Bressi S, Della Sala S, Logie R, Spinnler H (1991) The decline of working memory in Alzheimer’s disease. A longitudinal study. Brain 114(pt 6):2521–2542

    Article  PubMed  Google Scholar 

  • Brown RG, Marsden CD (1988) Internal versus external cues and the control of attention in Parkinson’s disease. Brain 111(Pt 2):323–345

    Article  PubMed  Google Scholar 

  • Brown RG, Marsden CD (1991) Dual task performance and processing resources in normal subjects and patients with Parkinson’s disease. Brain 114(Pt 1A):215–231

    PubMed  Google Scholar 

  • Chikazoe J (2010) Localizing performance of go/no-go tasks to prefrontal cortical subregions. Curr Opin Psychiatry 23(3):267–272. doi:10.1097/YCO.0b013e3283387a9f

    Article  PubMed  Google Scholar 

  • Christofoletti G, Andrade LP, Beinotti F, Borges G (2014) Cognition and dual-task performance in older adults with Parkinson’s and Alzheimer’s disease. Int J Gen Med 7:383–388. doi:10.2147/IJGM.S65803

    Article  PubMed Central  PubMed  Google Scholar 

  • Cummings JL (1988) Intellectual impairment in Parkinson’s disease: clinical, pathologic, and biochemical correlates. J Geriatr Psychiatry Neurol 1(1):24–36

    Article  CAS  PubMed  Google Scholar 

  • Dirnberger G, Jahanshahi M (2013) Executive dysfunction in Parkinson’s disease: a review. J Neuropsychol 7(2):193–224. doi:10.1111/jnp.12028

    Article  PubMed  Google Scholar 

  • Emre M (2003) Dementia associated with Parkinson’s disease. Lancet Neurol 2(4):229–237

    Article  CAS  PubMed  Google Scholar 

  • Foley JA, Kaschel R, Logie RH, Della Sala S (2011) Dual-task performance in Alzheimer’s disease, mild cognitive impairment, and normal ageing. Arch Clin Neuropsychol 26(4):340–348. doi:10.1093/arclin/acr032

    Article  PubMed  Google Scholar 

  • Foley JA, Kaschel R, Sala SD (2013) Dual task performance in Parkinson’s disease. Behav Neurol 27(2):183–191. doi:10.3233/BEN-110238

    Article  PubMed  Google Scholar 

  • 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(3):189–198

    Article  CAS  PubMed  Google Scholar 

  • Girotti F, Soliveri P, Carella F, Piccolo I, Caffarra P, Musicco M, Caraceni T (1988) Dementia and cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry 51(12):1498–1502

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17(5):427–442

    Article  CAS  PubMed  Google Scholar 

  • 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(3):181–184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kelly VE, Eusterbrock AJ, Shumway-Cook A (2012) A review of dual-task walking deficits in people with Parkinson’s disease: motor and cognitive contributions, mechanisms, and clinical implications. Parkinson’s Dis 2012:918719. doi:10.1155/2012/918719

    Google Scholar 

  • Litvan I, Mohr E, Williams J, Gomez C, Chase TN (1991) Differential memory and executive functions in demented patients with Parkinson’s and Alzheimer’s disease. J Neurol Neurosurg Psychiatry 54(1):25–29

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Logie RH, Cocchini G, Delia Sala S, Baddeley AD (2004) Is there a specific executive capacity for dual task coordination? Evidence from Alzheimer’s disease. Neuropsychology 18(3):504–513. doi:10.1037/0894-4105.18.3.504

    Article  PubMed  Google Scholar 

  • Lord S, Rochester L, Hetherington V, Allcock LM, Burn D (2010) Executive dysfunction and attention contribute to gait interference in ‘off’ state Parkinson’s disease. Gait Posture 31(2):169–174. doi:10.1016/j.gaitpost.2009.09.019

    Article  PubMed  Google Scholar 

  • MacPherson SE, Della Sala S, Logie RH, Wilcock GK (2007) Specific AD impairment in concurrent performance of two memory tasks. Cortex 43(7):858–865

    Article  PubMed  Google Scholar 

  • Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65(8):1239–1245. doi:10.1212/01.wnl.0000180516.69442.95

    Article  PubMed  Google Scholar 

  • Obeso I, Wilkinson L, Casabona E, Bringas ML, Alvarez M, Alvarez L, Pavon N, Rodriguez-Oroz MC, Macias R, Obeso JA, Jahanshahi M (2011) Deficits in inhibitory control and conflict resolution on cognitive and motor tasks in Parkinson’s disease. Exp Brain Res 212(3):371–384. doi:10.1007/s00221-011-2736-6

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Pillon B, Dubois B, Lhermitte F, Agid Y (1986) Heterogeneity of cognitive impairment in progressive supranuclear palsy, Parkinson’s disease, and Alzheimer’s disease. Neurology 36(9):1179–1185

    Article  CAS  PubMed  Google Scholar 

  • Pillon B, Dubois B, Ploska A, Agid Y (1991) Severity and specificity of cognitive impairment in Alzheimer’s, Huntington’s, and Parkinson’s diseases and progressive supranuclear palsy. Neurology 41(5):634–643

    Article  CAS  PubMed  Google Scholar 

  • Plotnik M, Dagan Y, Gurevich T, Giladi N, Hausdorff JM (2011a) Effects of cognitive function on gait and dual tasking abilities in patients with Parkinson’s disease suffering from motor response fluctuations. Exp Brain Res 208(2):169–179. doi:10.1007/s00221-010-2469-y

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Dagan Y, Hausdorff JM (2011b) Postural instability and fall risk in Parkinson’s disease: impaired dual tasking, pacing, and bilateral coordination of gait during the “ON” medication state. Exp Brain Res 210(3–4):529–538. doi:10.1007/s00221-011-2551-0

    Article  PubMed  Google Scholar 

  • Ratcliff R, McKoon G (2008) The diffusion decision model: theory and data for two-choice decision tasks. Neural Comput 20(4):873–922. doi:10.1162/neco.2008.12-06-420

    Article  PubMed Central  PubMed  Google Scholar 

  • Shallice T, Burgess P (1996) The domain of supervisory processes and temporal organization of behaviour. Philos Trans R Soc Lond Ser B Biol Sci 351(1346):1405–1411. doi:10.1098/rstb.1996.0124 (discussion 1411–1402)

    Article  CAS  Google Scholar 

  • Vriend C, Gerrits NJ, Berendse HW, Veltman DJ, van den Heuvel OA, van der Werf YD (2014) Failure of stop and go in de novo Parkinson’s disease-a functional magnetic resonance imaging study. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2014.07.031

    PubMed  Google Scholar 

  • Wild LB, de Lima DB, Balardin JB, Rizzi L, Giacobbo BL, Oliveira HB, deLima A, Peyre-Tartaruga LA, Rieder CR, Bromberg E (2013) Characterization of cognitive and motor performance during dual-tasking in healthy older adults and patients with Parkinson’s disease. J Neurol 260(2):580–589. doi:10.1007/s00415-012-6683-3

    Article  PubMed  Google Scholar 

  • Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130(Pt 7):1787–1798. doi:10.1093/brain/awm111

    Article  CAS  PubMed  Google Scholar 

  • Woodward TS, Bub DN, Hunter MA (2002) Task switching deficits associated with Parkinson’s disease reflect depleted attentional resources. Neuropsychologia 40(12):1948–1955

    Article  PubMed  Google Scholar 

  • Wu T, Hallett M (2008) Neural correlates of dual task performance in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 79(7):760–766. doi:10.1136/jnnp.2007.126599

    Article  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Charité, University Medicine Berlin, Berlin, Germany

    Frank Marzinzik, Anja Herrmann, Jacob H. Gogarten, Andreas Lueschow, Joachim E. Weber, Katharina A. Schindlbeck & Fabian Klostermann

Authors
  1. Frank Marzinzik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anja Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacob H. Gogarten
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andreas Lueschow
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joachim E. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katharina A. Schindlbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fabian Klostermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frank Marzinzik.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marzinzik, F., Herrmann, A., Gogarten, J.H. et al. Dysfunctional action control as a specific feature of Parkinson’s disease. J Neural Transm 122, 1125–1133 (2015). https://doi.org/10.1007/s00702-014-1354-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-014-1354-4

Keywords

Search

Navigation