Cerebral activations related to ballistic, stepwise interrupted and gradually modulated movements in parkinson patients

Carolien M. Toxopeus, Natasha M. Maurits, Klaus L. Leenders, Bauke M. de Jong, Gopal Valsan, Bernard A. Conway

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Patients with Parkinson's disease (PD) experience impaired initiation and inhibition of movements such as difficulty to start/stop walking. At single-joint level this is accompanied by reduced inhibition of antagonist muscle activity. While normal basal ganglia (BG) contributions to motor control include selecting appropriate muscles by inhibiting others, it is unclear how PD-related changes in BG function cause impaired movement initiation and inhibition at single-joint level. To further elucidate these changes we studied 4 right-hand movement tasks with fMRI, by dissociating activations related to abrupt movement initiation, inhibition and gradual movement modulation. Initiation and inhibition were inferred from ballistic and stepwise interrupted movement, respectively, while smooth wrist circumduction enabled the assessment of gradually modulated movement. Task-related activations were compared between PD patients (N = 12) and healthy subjects (N = 18). In healthy subjects, movement initiation was characterized by antero-ventral striatum, substantia nigra (SN) and premotor activations while inhibition was dominated by subthalamic nucleus (STN) and pallidal activations, in line with the known role of these areas in simple movement. Gradual movement mainly involved antero-dorsal putamen and pallidum. Compared to healthy subjects, patients showed reduced striatal/SN and increased pallidal activation for initiation, whereas for inhibition STN activation was reduced and striatal-thalamo-cortical activation increased. For gradual movement patients showed reduced pallidal and increased thalamo-cortical activation. We conclude that PD-related changes during movement initiation fit the (rather static) model of alterations in direct and indirect BG pathways. Reduced STN activation and regional cortical increased activation in PD during inhibition and gradual movement modulation are better explained by a dynamic model that also takes into account enhanced responsiveness to external stimuli in this disease and the effects of hyper-fluctuating cortical inputs to the striatum and STN in particular.

LanguageEnglish
Article numbere41042
Number of pages15
JournalPLOS One
Volume7
Issue number7
DOIs
Publication statusPublished - 23 Jul 2012

Fingerprint

Parkinson disease
Ballistics
Subthalamic Nucleus
Parkinson Disease
Chemical activation
Basal Ganglia
Corpus Striatum
Healthy Volunteers
Substantia Nigra
joints (animal)
Joints
Muscles
muscles
Globus Pallidus
Putamen
Wrist
dynamic models
walking
Walking
Muscle

Keywords

  • cerebral activations
  • ballistic
  • stepwise
  • interrupted
  • gradually modulated movements
  • parkinson patients

Cite this

Toxopeus, Carolien M. ; Maurits, Natasha M. ; Leenders, Klaus L. ; de Jong, Bauke M. ; Valsan, Gopal ; Conway, Bernard A. / Cerebral activations related to ballistic, stepwise interrupted and gradually modulated movements in parkinson patients. In: PLOS One. 2012 ; Vol. 7, No. 7.
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abstract = "Patients with Parkinson's disease (PD) experience impaired initiation and inhibition of movements such as difficulty to start/stop walking. At single-joint level this is accompanied by reduced inhibition of antagonist muscle activity. While normal basal ganglia (BG) contributions to motor control include selecting appropriate muscles by inhibiting others, it is unclear how PD-related changes in BG function cause impaired movement initiation and inhibition at single-joint level. To further elucidate these changes we studied 4 right-hand movement tasks with fMRI, by dissociating activations related to abrupt movement initiation, inhibition and gradual movement modulation. Initiation and inhibition were inferred from ballistic and stepwise interrupted movement, respectively, while smooth wrist circumduction enabled the assessment of gradually modulated movement. Task-related activations were compared between PD patients (N = 12) and healthy subjects (N = 18). In healthy subjects, movement initiation was characterized by antero-ventral striatum, substantia nigra (SN) and premotor activations while inhibition was dominated by subthalamic nucleus (STN) and pallidal activations, in line with the known role of these areas in simple movement. Gradual movement mainly involved antero-dorsal putamen and pallidum. Compared to healthy subjects, patients showed reduced striatal/SN and increased pallidal activation for initiation, whereas for inhibition STN activation was reduced and striatal-thalamo-cortical activation increased. For gradual movement patients showed reduced pallidal and increased thalamo-cortical activation. We conclude that PD-related changes during movement initiation fit the (rather static) model of alterations in direct and indirect BG pathways. Reduced STN activation and regional cortical increased activation in PD during inhibition and gradual movement modulation are better explained by a dynamic model that also takes into account enhanced responsiveness to external stimuli in this disease and the effects of hyper-fluctuating cortical inputs to the striatum and STN in particular.",
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Cerebral activations related to ballistic, stepwise interrupted and gradually modulated movements in parkinson patients. / Toxopeus, Carolien M.; Maurits, Natasha M.; Leenders, Klaus L.; de Jong, Bauke M.; Valsan, Gopal; Conway, Bernard A.

In: PLOS One, Vol. 7, No. 7, e41042, 23.07.2012.

Research output: Contribution to journalArticle

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AU - Toxopeus, Carolien M.

AU - Maurits, Natasha M.

AU - Leenders, Klaus L.

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AU - Valsan, Gopal

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