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The Journal of Neuroscience, March 1, 2003, 23(5):1916
Stimulation of the Subthalamic Nucleus Changes the Firing Pattern
of Pallidal Neurons
Takao
Hashimoto1, 2,
Christopher M.
Elder1,
Michael S.
Okun1,
Susan K.
Patrick1, and
Jerrold L.
Vitek1
1 Department of Neurology, Emory University School of
Medicine, Atlanta, Georgia 30322, and 2 Third Department of
Medicine, Shinshu University School of Medicine, Matsumoto 390-8621, Japan
To clarify the mechanism underlying improvement of parkinsonian
signs by high-frequency electrical stimulation (HFS) of the subthalamic
nucleus (STN), we investigated the effects of STN HFS on neuronal
activity of the internal and external segment of the globus pallidus
(GPi and GPe, respectively) in two rhesus monkeys rendered parkinsonian
by administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. A
scaled-down version of the chronic stimulating electrode used in
humans, consisting of four metal contacts 0.50 mm in length each
separated by 0.50 mm, was implanted through a cephalic chamber targeting the STN. Histological reconstruction revealed that the cathode was located in the STN in both monkeys. Extracellular recordings from a total of 110 pallidal neurons during STN stimulation were performed. Poststimulus time histograms of single neurons triggered by 2 Hz STN stimulation pulses at 2.4-3.0 V revealed short-latency excitations at 2.5-4.5 and 5.5-7.0 msec after
stimulation onset and inhibitions at 1.0-2.5, 4.5-5.5, and 7.0-9.0
msec for both GPe and GPi neurons. These short-latency responses were
present with 136 Hz stimulation, at voltages effective for alleviation of parkinsonian signs, resulting in a significant increase in mean
discharge rate and a stimulus-synchronized regular firing pattern.
These results indicate that activation of the STN efferent fibers and
resultant changes in the temporal firing pattern of neurons in GPe and
GPi underlie the beneficial effect of HFS in the STN in Parkinson's
disease and further support the role of temporal firing patterns in the
basal ganglia in the development of Parkinson's disease and other
movement disorders.
Key words:
subthalamic nucleus; globus pallidus; Parkinson's
disease; MPTP; deep brain stimulation; motor circuit
Copyright © 2003 Society for Neuroscience 0270-6474/03/2351916-08$05.00/0
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|
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|
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|
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|
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|
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|
 |
|

|
 |

|
 |
 
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|
 |
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|
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|
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|
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|
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|
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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127(9):
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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24(33):
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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559(1):
301 - 313.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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August 1, 2004;
127(8):
1899 - 1908.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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April 1, 2004;
309(1):
1 - 7.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
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April 1, 2004;
91(4):
1457 - 1469.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Effects of deep brain stimulation and medication on bradykinesia and muscle activation in Parkinson's disease
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March 1, 2004;
127(3):
491 - 504.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Subthalamic nucleus stimulation modulates motor cortex oscillatory activity in Parkinson's disease
Brain,
February 1, 2004;
127(2):
408 - 419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Effects of High-Frequency Stimulation on Subthalamic Neuronal Activity in Parkinsonian Patients
Arch Neurol,
January 1, 2004;
61(1):
89 - 96.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Hamani, J. A. Saint-Cyr, J. Fraser, M. Kaplitt, and A. M. Lozano
The subthalamic nucleus in the context of movement disorders
Brain,
January 1, 2004;
127(1):
4 - 20.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Involvement of the human subthalamic nucleus in movement preparation
Neurology,
December 9, 2003;
61(11):
1538 - 1545.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Globus Pallidus Discharge Is Coincident with Striatal Activity during Global Slow Wave Activity in the Rat
J. Neurosci.,
November 5, 2003;
23(31):
10058 - 10063.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Spontaneous and Evoked Activity of Substantia Nigra Pars Reticulata Neurons during High-Frequency Stimulation of the Subthalamic Nucleus
J. Neurosci.,
October 29, 2003;
23(30):
9929 - 9936.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Electrophysiological and metabolic evidence that high-frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata
FASEB J,
October 1, 2003;
17(13):
1820 - 1830.
[Abstract]
[Full Text]
[PDF]
|
 |
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|
 |

|
 |
 
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300-Hz subthalamic oscillations in Parkinson's disease
Brain,
October 1, 2003;
126(10):
2153 - 2163.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
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|
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Dual Effect of High-Frequency Stimulation on Subthalamic Neuron Activity
J. Neurosci.,
September 24, 2003;
23(25):
8743 - 8751.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Cortical and subcortical blood flow effects of subthalamic nucleus stimulation in PD
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September 23, 2003;
61(6):
816 - 821.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|