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Potential mechanisms for imperfect synchronization in parkinsonian basal ganglia.

Park C, Rubchinsky LL - PLoS ONE (2012)

Bottom Line: However, dopamine also affects the cellular properties of neurons.The intermittent nature of the neural beta band synchrony in Parkinson's disease is achieved in the model due to the interplay of the timing of STN input to pallidum and pallidal neuronal dynamics, resulting in sensitivity of pallidal output to the phase of the arriving STN input.Thus the mechanism considered here (the change in firing pattern of subthalamic neurons through the dopamine-induced change of membrane properties) may be one of the potential mechanisms responsible for the generation of the intermittent synchronization observed in Parkinson's disease.

View Article: PubMed Central - PubMed

Affiliation: Department of Mathematical Sciences and Center for Mathematical Biosciences, Indiana University Purdue University Indianapolis, Indianapolis, IN, USA. 21cspark@gmail.com

ABSTRACT
Neural activity in the brain of parkinsonian patients is characterized by the intermittently synchronized oscillatory dynamics. This imperfect synchronization, observed in the beta frequency band, is believed to be related to the hypokinetic motor symptoms of the disorder. Our study explores potential mechanisms behind this intermittent synchrony. We study the response of a bursting pallidal neuron to different patterns of synaptic input from subthalamic nucleus (STN) neuron. We show how external globus pallidus (GPe) neuron is sensitive to the phase of the input from the STN cell and can exhibit intermittent phase-locking with the input in the beta band. The temporal properties of this intermittent phase-locking show similarities to the intermittent synchronization observed in experiments. We also study the synchronization of GPe cells to synaptic input from the STN cell with dependence on the dopamine-modulated parameters. Earlier studies showed how the strengthening of dopamine-modulated coupling may lead to transitions from non-synchronized to partially synchronized dynamics, typical in Parkinson's disease. However, dopamine also affects the cellular properties of neurons. We show how the changes in firing patterns of STN neuron due to the lack of dopamine may lead to transition from a lower to a higher coherent state, roughly matching the synchrony levels observed in basal ganglia in normal and parkinsonian states. The intermittent nature of the neural beta band synchrony in Parkinson's disease is achieved in the model due to the interplay of the timing of STN input to pallidum and pallidal neuronal dynamics, resulting in sensitivity of pallidal output to the phase of the arriving STN input. Thus the mechanism considered here (the change in firing pattern of subthalamic neurons through the dopamine-induced change of membrane properties) may be one of the potential mechanisms responsible for the generation of the intermittent synchronization observed in Parkinson's disease.

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Transition between low and high coherence.A) An example of projection of a 2-dimensional surface in a parameter space onto -ISI plane, which shows a transition from weakly coherent to stronger coherent states. Right bar shows the level of phase-locking index . B) We chose one trajectory from upper left corner (low coherence) to lower right corner (high coherence) to illustrate coherence transition. Numbers (1 to 12) within (A) represent the labels of the points chosen. These numbers are used in a horizontal axis in (B).
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pone-0051530-g009: Transition between low and high coherence.A) An example of projection of a 2-dimensional surface in a parameter space onto -ISI plane, which shows a transition from weakly coherent to stronger coherent states. Right bar shows the level of phase-locking index . B) We chose one trajectory from upper left corner (low coherence) to lower right corner (high coherence) to illustrate coherence transition. Numbers (1 to 12) within (A) represent the labels of the points chosen. These numbers are used in a horizontal axis in (B).

Mentions: Figure 8 suggests that we might get a 2-dimensional surface in 3-dimensional parameter space which shows a transition from low coherence state to high coherence state. Figure 9A provides one example of such a surface projected onto (, )-plane. To get a transition from high coherence state (lower right region) to low coherence state (upper left region), we should increase ISI and . For each (, ) value, we have a different value. In general, decreases monotonically along the horizontal or vertical lines in (ISI, )-plane. Over the lower synchrony area / is around 0.3; it is around 0.15 over the higher synchrony region. Along the diagonal band from lower right region to upper left region, we have overall increase of . We chose one route from the upper left to lower right area along the diagonal band and plotted the corresponding averaged phase synchrony index γ in Figure 9B. We can see a relatively smooth transition from lower to higher synchrony level. Along that trajectory, the number of spikes per burst increases from 2 to 3 and the mean / is 0.3 over the first 5 points and 0.216 over the last 5 points.


Potential mechanisms for imperfect synchronization in parkinsonian basal ganglia.

Park C, Rubchinsky LL - PLoS ONE (2012)

Transition between low and high coherence.A) An example of projection of a 2-dimensional surface in a parameter space onto -ISI plane, which shows a transition from weakly coherent to stronger coherent states. Right bar shows the level of phase-locking index . B) We chose one trajectory from upper left corner (low coherence) to lower right corner (high coherence) to illustrate coherence transition. Numbers (1 to 12) within (A) represent the labels of the points chosen. These numbers are used in a horizontal axis in (B).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3526636&req=5

pone-0051530-g009: Transition between low and high coherence.A) An example of projection of a 2-dimensional surface in a parameter space onto -ISI plane, which shows a transition from weakly coherent to stronger coherent states. Right bar shows the level of phase-locking index . B) We chose one trajectory from upper left corner (low coherence) to lower right corner (high coherence) to illustrate coherence transition. Numbers (1 to 12) within (A) represent the labels of the points chosen. These numbers are used in a horizontal axis in (B).
Mentions: Figure 8 suggests that we might get a 2-dimensional surface in 3-dimensional parameter space which shows a transition from low coherence state to high coherence state. Figure 9A provides one example of such a surface projected onto (, )-plane. To get a transition from high coherence state (lower right region) to low coherence state (upper left region), we should increase ISI and . For each (, ) value, we have a different value. In general, decreases monotonically along the horizontal or vertical lines in (ISI, )-plane. Over the lower synchrony area / is around 0.3; it is around 0.15 over the higher synchrony region. Along the diagonal band from lower right region to upper left region, we have overall increase of . We chose one route from the upper left to lower right area along the diagonal band and plotted the corresponding averaged phase synchrony index γ in Figure 9B. We can see a relatively smooth transition from lower to higher synchrony level. Along that trajectory, the number of spikes per burst increases from 2 to 3 and the mean / is 0.3 over the first 5 points and 0.216 over the last 5 points.

Bottom Line: However, dopamine also affects the cellular properties of neurons.The intermittent nature of the neural beta band synchrony in Parkinson's disease is achieved in the model due to the interplay of the timing of STN input to pallidum and pallidal neuronal dynamics, resulting in sensitivity of pallidal output to the phase of the arriving STN input.Thus the mechanism considered here (the change in firing pattern of subthalamic neurons through the dopamine-induced change of membrane properties) may be one of the potential mechanisms responsible for the generation of the intermittent synchronization observed in Parkinson's disease.

View Article: PubMed Central - PubMed

Affiliation: Department of Mathematical Sciences and Center for Mathematical Biosciences, Indiana University Purdue University Indianapolis, Indianapolis, IN, USA. 21cspark@gmail.com

ABSTRACT
Neural activity in the brain of parkinsonian patients is characterized by the intermittently synchronized oscillatory dynamics. This imperfect synchronization, observed in the beta frequency band, is believed to be related to the hypokinetic motor symptoms of the disorder. Our study explores potential mechanisms behind this intermittent synchrony. We study the response of a bursting pallidal neuron to different patterns of synaptic input from subthalamic nucleus (STN) neuron. We show how external globus pallidus (GPe) neuron is sensitive to the phase of the input from the STN cell and can exhibit intermittent phase-locking with the input in the beta band. The temporal properties of this intermittent phase-locking show similarities to the intermittent synchronization observed in experiments. We also study the synchronization of GPe cells to synaptic input from the STN cell with dependence on the dopamine-modulated parameters. Earlier studies showed how the strengthening of dopamine-modulated coupling may lead to transitions from non-synchronized to partially synchronized dynamics, typical in Parkinson's disease. However, dopamine also affects the cellular properties of neurons. We show how the changes in firing patterns of STN neuron due to the lack of dopamine may lead to transition from a lower to a higher coherent state, roughly matching the synchrony levels observed in basal ganglia in normal and parkinsonian states. The intermittent nature of the neural beta band synchrony in Parkinson's disease is achieved in the model due to the interplay of the timing of STN input to pallidum and pallidal neuronal dynamics, resulting in sensitivity of pallidal output to the phase of the arriving STN input. Thus the mechanism considered here (the change in firing pattern of subthalamic neurons through the dopamine-induced change of membrane properties) may be one of the potential mechanisms responsible for the generation of the intermittent synchronization observed in Parkinson's disease.

Show MeSH
Related in: MedlinePlus