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Articles, Neurobiology of Disease

Disrupted Dopamine Transmission and the Emergence of Exaggerated Beta Oscillations in Subthalamic Nucleus and Cerebral Cortex

Nicolas Mallet, Alek Pogosyan, Andrew Sharott, Jozsef Csicsvari, J. Paul Bolam, Peter Brown and Peter J. Magill
Journal of Neuroscience 30 April 2008, 28 (18) 4795-4806; DOI: https://doi.org/10.1523/JNEUROSCI.0123-08.2008
Nicolas Mallet
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Alek Pogosyan
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Andrew Sharott
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Jozsef Csicsvari
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J. Paul Bolam
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Peter Brown
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Peter J. Magill
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Abstract

In the subthalamic nucleus (STN) of Parkinson's disease (PD) patients, a pronounced synchronization of oscillatory activity at beta frequencies (15–30 Hz) accompanies movement difficulties. Abnormal beta oscillations and motor symptoms are concomitantly and acutely suppressed by dopaminergic therapies, suggesting that these inappropriate rhythms might also emerge acutely from disrupted dopamine transmission. The neural basis of these abnormal beta oscillations is unclear, and how they might compromise information processing, or how they arise, is unknown. Using a 6-hydroxydopamine-lesioned rodent model of PD, we demonstrate that beta oscillations are inappropriately exaggerated, compared with controls, in a brain-state-dependent manner after chronic dopamine loss. Exaggerated beta oscillations are expressed at the levels of single neurons and small neuronal ensembles, and are focally present and spatially distributed within STN. They are also expressed in synchronous population activities, as evinced by oscillatory local field potentials, in STN and cortex. Excessively synchronized beta oscillations reduce the information coding capacity of STN neuronal ensembles, which may contribute to parkinsonian motor impairment. Acute disruption of dopamine transmission in control animals with antagonists of D1/D2 receptors did not exaggerate STN or cortical beta oscillations. Moreover, beta oscillations were not exaggerated until several days after 6-hydroxydopamine injections. Thus, contrary to predictions, abnormally amplified beta oscillations in cortico-STN circuits do not result simply from an acute absence of dopamine receptor stimulation, but are instead delayed sequelae of chronic dopamine depletion. Targeting the plastic processes underlying the delayed emergence of pathological beta oscillations after continuing dopaminergic dysfunction may offer considerable therapeutic promise.

  • subthalamic nucleus
  • cerebral cortex
  • basal ganglia
  • Parkinson's disease
  • dopamine
  • 6-hydroxydopamine
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The Journal of Neuroscience: 28 (18)
Journal of Neuroscience
Vol. 28, Issue 18
30 Apr 2008
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Disrupted Dopamine Transmission and the Emergence of Exaggerated Beta Oscillations in Subthalamic Nucleus and Cerebral Cortex
Nicolas Mallet, Alek Pogosyan, Andrew Sharott, Jozsef Csicsvari, J. Paul Bolam, Peter Brown, Peter J. Magill
Journal of Neuroscience 30 April 2008, 28 (18) 4795-4806; DOI: 10.1523/JNEUROSCI.0123-08.2008

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Disrupted Dopamine Transmission and the Emergence of Exaggerated Beta Oscillations in Subthalamic Nucleus and Cerebral Cortex
Nicolas Mallet, Alek Pogosyan, Andrew Sharott, Jozsef Csicsvari, J. Paul Bolam, Peter Brown, Peter J. Magill
Journal of Neuroscience 30 April 2008, 28 (18) 4795-4806; DOI: 10.1523/JNEUROSCI.0123-08.2008
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