The effects of cues on neurons in the basal ganglia in Parkinson's disease

Sridevi V. Sarma, Ming L. Cheng, Uri Eden, Ziv Williams, Emery N. Brown, Emad N. Eskandar

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Visual cues open a unique window to the understanding of Parkinson's disease (PD). These cues can temporarily but dramatically improve PD motor symptoms. Although details are unclear, cues are believed to suppress pathological basal ganglia (BG) activity through activation of corticostriatal pathways. In this study, we investigated human BG neurophysiology under different cued conditions. We evaluated bursting, 10-30 Hz oscillations (OSCs), and directional tuning (DT) dynamics in the subthalamic nucleus (STN) activity while seven patients executed a two-step motor task. In the first step (predicted +cue), the patient moved to a target when prompted by a visual go cue that appeared 100% of the time. Here, the timing of the cue is predictable and the cue serves an external trigger to execute a motor plan. In the second step, the cue appeared randomly 50% of the time, and the patient had to move to the same target as in the first step. When it appeared (unpredicted +cue), the motor plan was to be triggered by the cue, but its timing was not predictable. When the cue failed to appear (unpredicted -cue), the motor plan was triggered by the absence of the visual cue. We found that during predicted +cue and unpredicted -cue trials, OSCs significantly decreased and DT significantly increased above baseline, though these modulations occurred an average of 640 ms later in unpredicted -cue trials. Movement and reaction times were comparable in these trials. During unpredicted +cue trials, OSCs, and DT failed to modulate though bursting significantly decreased after movement. Correspondingly, movement performance deteriorated. These findings suggest that during motor planning either a predictably timed external cue or an internally generated cue (generated by the absence of a cue) trigger the execution of a motor plan in premotor cortex, whose increased activation then suppresses pathological activity in STN through direct pathways, leading to motor facilitation in PD.

Original languageEnglish (US)
JournalFrontiers in Integrative Neuroscience
Issue numberJULY 2012
DOIs
StatePublished - Jul 26 2012
Externally publishedYes

Fingerprint

Basal Ganglia
Cues
Parkinson Disease
Neurons
Subthalamic Nucleus
Neurophysiology
Motor Cortex

Keywords

  • Cueing
  • Neuromodulation
  • Neuron
  • Neuropathology
  • Parkinson disease

ASJC Scopus subject areas

  • Sensory Systems
  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

Cite this

The effects of cues on neurons in the basal ganglia in Parkinson's disease. / Sarma, Sridevi V.; Cheng, Ming L.; Eden, Uri; Williams, Ziv; Brown, Emery N.; Eskandar, Emad N.

In: Frontiers in Integrative Neuroscience, No. JULY 2012, 26.07.2012.

Research output: Contribution to journalArticle

Sarma, Sridevi V. ; Cheng, Ming L. ; Eden, Uri ; Williams, Ziv ; Brown, Emery N. ; Eskandar, Emad N. / The effects of cues on neurons in the basal ganglia in Parkinson's disease. In: Frontiers in Integrative Neuroscience. 2012 ; No. JULY 2012.
@article{5ce4df47af1145b18389e906b6ffa8bd,
title = "The effects of cues on neurons in the basal ganglia in Parkinson's disease",
abstract = "Visual cues open a unique window to the understanding of Parkinson's disease (PD). These cues can temporarily but dramatically improve PD motor symptoms. Although details are unclear, cues are believed to suppress pathological basal ganglia (BG) activity through activation of corticostriatal pathways. In this study, we investigated human BG neurophysiology under different cued conditions. We evaluated bursting, 10-30 Hz oscillations (OSCs), and directional tuning (DT) dynamics in the subthalamic nucleus (STN) activity while seven patients executed a two-step motor task. In the first step (predicted +cue), the patient moved to a target when prompted by a visual go cue that appeared 100{\%} of the time. Here, the timing of the cue is predictable and the cue serves an external trigger to execute a motor plan. In the second step, the cue appeared randomly 50{\%} of the time, and the patient had to move to the same target as in the first step. When it appeared (unpredicted +cue), the motor plan was to be triggered by the cue, but its timing was not predictable. When the cue failed to appear (unpredicted -cue), the motor plan was triggered by the absence of the visual cue. We found that during predicted +cue and unpredicted -cue trials, OSCs significantly decreased and DT significantly increased above baseline, though these modulations occurred an average of 640 ms later in unpredicted -cue trials. Movement and reaction times were comparable in these trials. During unpredicted +cue trials, OSCs, and DT failed to modulate though bursting significantly decreased after movement. Correspondingly, movement performance deteriorated. These findings suggest that during motor planning either a predictably timed external cue or an internally generated cue (generated by the absence of a cue) trigger the execution of a motor plan in premotor cortex, whose increased activation then suppresses pathological activity in STN through direct pathways, leading to motor facilitation in PD.",
keywords = "Cueing, Neuromodulation, Neuron, Neuropathology, Parkinson disease",
author = "Sarma, {Sridevi V.} and Cheng, {Ming L.} and Uri Eden and Ziv Williams and Brown, {Emery N.} and Eskandar, {Emad N.}",
year = "2012",
month = "7",
day = "26",
doi = "10.3389/fnint.2012.00040",
language = "English (US)",
journal = "Frontiers in Integrative Neuroscience",
issn = "1662-5145",
publisher = "Frontiers Research Foundation",
number = "JULY 2012",

}

TY - JOUR

T1 - The effects of cues on neurons in the basal ganglia in Parkinson's disease

AU - Sarma, Sridevi V.

AU - Cheng, Ming L.

AU - Eden, Uri

AU - Williams, Ziv

AU - Brown, Emery N.

AU - Eskandar, Emad N.

PY - 2012/7/26

Y1 - 2012/7/26

N2 - Visual cues open a unique window to the understanding of Parkinson's disease (PD). These cues can temporarily but dramatically improve PD motor symptoms. Although details are unclear, cues are believed to suppress pathological basal ganglia (BG) activity through activation of corticostriatal pathways. In this study, we investigated human BG neurophysiology under different cued conditions. We evaluated bursting, 10-30 Hz oscillations (OSCs), and directional tuning (DT) dynamics in the subthalamic nucleus (STN) activity while seven patients executed a two-step motor task. In the first step (predicted +cue), the patient moved to a target when prompted by a visual go cue that appeared 100% of the time. Here, the timing of the cue is predictable and the cue serves an external trigger to execute a motor plan. In the second step, the cue appeared randomly 50% of the time, and the patient had to move to the same target as in the first step. When it appeared (unpredicted +cue), the motor plan was to be triggered by the cue, but its timing was not predictable. When the cue failed to appear (unpredicted -cue), the motor plan was triggered by the absence of the visual cue. We found that during predicted +cue and unpredicted -cue trials, OSCs significantly decreased and DT significantly increased above baseline, though these modulations occurred an average of 640 ms later in unpredicted -cue trials. Movement and reaction times were comparable in these trials. During unpredicted +cue trials, OSCs, and DT failed to modulate though bursting significantly decreased after movement. Correspondingly, movement performance deteriorated. These findings suggest that during motor planning either a predictably timed external cue or an internally generated cue (generated by the absence of a cue) trigger the execution of a motor plan in premotor cortex, whose increased activation then suppresses pathological activity in STN through direct pathways, leading to motor facilitation in PD.

AB - Visual cues open a unique window to the understanding of Parkinson's disease (PD). These cues can temporarily but dramatically improve PD motor symptoms. Although details are unclear, cues are believed to suppress pathological basal ganglia (BG) activity through activation of corticostriatal pathways. In this study, we investigated human BG neurophysiology under different cued conditions. We evaluated bursting, 10-30 Hz oscillations (OSCs), and directional tuning (DT) dynamics in the subthalamic nucleus (STN) activity while seven patients executed a two-step motor task. In the first step (predicted +cue), the patient moved to a target when prompted by a visual go cue that appeared 100% of the time. Here, the timing of the cue is predictable and the cue serves an external trigger to execute a motor plan. In the second step, the cue appeared randomly 50% of the time, and the patient had to move to the same target as in the first step. When it appeared (unpredicted +cue), the motor plan was to be triggered by the cue, but its timing was not predictable. When the cue failed to appear (unpredicted -cue), the motor plan was triggered by the absence of the visual cue. We found that during predicted +cue and unpredicted -cue trials, OSCs significantly decreased and DT significantly increased above baseline, though these modulations occurred an average of 640 ms later in unpredicted -cue trials. Movement and reaction times were comparable in these trials. During unpredicted +cue trials, OSCs, and DT failed to modulate though bursting significantly decreased after movement. Correspondingly, movement performance deteriorated. These findings suggest that during motor planning either a predictably timed external cue or an internally generated cue (generated by the absence of a cue) trigger the execution of a motor plan in premotor cortex, whose increased activation then suppresses pathological activity in STN through direct pathways, leading to motor facilitation in PD.

KW - Cueing

KW - Neuromodulation

KW - Neuron

KW - Neuropathology

KW - Parkinson disease

UR - http://www.scopus.com/inward/record.url?scp=84865090327&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84865090327&partnerID=8YFLogxK

U2 - 10.3389/fnint.2012.00040

DO - 10.3389/fnint.2012.00040

M3 - Article

C2 - 22855673

AN - SCOPUS:84865090327

JO - Frontiers in Integrative Neuroscience

JF - Frontiers in Integrative Neuroscience

SN - 1662-5145

IS - JULY 2012

ER -