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Effects of dopamine depletion on network entropy in the external globus pallidus.

Cruz AV, Mallet N, Magill PJ, Brown P, Averbeck BB - J. Neurophysiol. (2009)

Bottom Line: Dopamine depletion led to decreases in the firing rates of GPe neurons and increases in synchronized network oscillations in the beta frequency (13-30 Hz) band.Changes in autocorrelations tended to offset these effects because autocorrelations decreased entropy more in the control animals.Thus it is possible that reduced information coding capacity within basal ganglia networks may contribute to the behavioral deficits accompanying PD.

View Article: PubMed Central - PubMed

Affiliation: Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom.

ABSTRACT
Dopamine depletion in cortical-basal ganglia circuits in Parkinson's disease (PD) grossly disturbs movement and cognition. Classic models relate Parkinsonian dysfunction to changes in firing rates of basal ganglia neurons. However, disturbances in other dynamics of neural activity are also common. Taking both inappropriate firing rates and other dynamics into account and determining how changes in the properties of these neural circuits that occur during PD impact on information coding are thus imperative. Here, we examined in vivo network dynamics in the external globus pallidus (GPe) of rats before and after chronic dopamine depletion. Dopamine depletion led to decreases in the firing rates of GPe neurons and increases in synchronized network oscillations in the beta frequency (13-30 Hz) band. Using logistic regression models, we determined the combined and separate impacts of these factors on network entropy, a measure of the upper bound of information coding capacity. Importantly, changes in these features in dopamine-depleted rats led to a significant decrease in GPe network entropy. Changes in firing rates had the largest impact on entropy, with changes in synchrony also decreasing entropy at the network level. Changes in autocorrelations tended to offset these effects because autocorrelations decreased entropy more in the control animals. Thus it is possible that reduced information coding capacity within basal ganglia networks may contribute to the behavioral deficits accompanying PD.

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Related in: MedlinePlus

Entropy per spike of full model. Data for all GPe neurons is shown, but entropy rate (H per spike) for each neuron was divided by the average firing rate of that neuron.
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f5: Entropy per spike of full model. Data for all GPe neurons is shown, but entropy rate (H per spike) for each neuron was divided by the average firing rate of that neuron.

Mentions: Entropy rate, i.e., entropy per second, as we calculated here, gives an estimate of the information capacity of the network and bounds how well the network can represent time-varying behaviors, for example, movements. Entropy per spike is a less direct measure of how well the network can code dynamic behaviors because it has to be multiplied by the spike rate to get an estimate of the information capacity per unit time. However, although entropy per spike is ultimately not the more relevant metric for understanding the coding capacity of the network, it is interesting from a theoretical, efficiency point of view (Rieke et al. 1995), particularly because the spike rates were lower in the lesioned animals, and the effects of the autocorrelations were larger in the control animals. We thus tested whether the entropy per spike (rather than per bin or per second) was similar in the two GPe networks. We found that the entropy per spike was actually lower in the controls compared with lesioned animals. As such, each individual spike of each GPe neuron carried more information in the lesioned animals (Fig. 5).


Effects of dopamine depletion on network entropy in the external globus pallidus.

Cruz AV, Mallet N, Magill PJ, Brown P, Averbeck BB - J. Neurophysiol. (2009)

Entropy per spike of full model. Data for all GPe neurons is shown, but entropy rate (H per spike) for each neuron was divided by the average firing rate of that neuron.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2724349&req=5

f5: Entropy per spike of full model. Data for all GPe neurons is shown, but entropy rate (H per spike) for each neuron was divided by the average firing rate of that neuron.
Mentions: Entropy rate, i.e., entropy per second, as we calculated here, gives an estimate of the information capacity of the network and bounds how well the network can represent time-varying behaviors, for example, movements. Entropy per spike is a less direct measure of how well the network can code dynamic behaviors because it has to be multiplied by the spike rate to get an estimate of the information capacity per unit time. However, although entropy per spike is ultimately not the more relevant metric for understanding the coding capacity of the network, it is interesting from a theoretical, efficiency point of view (Rieke et al. 1995), particularly because the spike rates were lower in the lesioned animals, and the effects of the autocorrelations were larger in the control animals. We thus tested whether the entropy per spike (rather than per bin or per second) was similar in the two GPe networks. We found that the entropy per spike was actually lower in the controls compared with lesioned animals. As such, each individual spike of each GPe neuron carried more information in the lesioned animals (Fig. 5).

Bottom Line: Dopamine depletion led to decreases in the firing rates of GPe neurons and increases in synchronized network oscillations in the beta frequency (13-30 Hz) band.Changes in autocorrelations tended to offset these effects because autocorrelations decreased entropy more in the control animals.Thus it is possible that reduced information coding capacity within basal ganglia networks may contribute to the behavioral deficits accompanying PD.

View Article: PubMed Central - PubMed

Affiliation: Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom.

ABSTRACT
Dopamine depletion in cortical-basal ganglia circuits in Parkinson's disease (PD) grossly disturbs movement and cognition. Classic models relate Parkinsonian dysfunction to changes in firing rates of basal ganglia neurons. However, disturbances in other dynamics of neural activity are also common. Taking both inappropriate firing rates and other dynamics into account and determining how changes in the properties of these neural circuits that occur during PD impact on information coding are thus imperative. Here, we examined in vivo network dynamics in the external globus pallidus (GPe) of rats before and after chronic dopamine depletion. Dopamine depletion led to decreases in the firing rates of GPe neurons and increases in synchronized network oscillations in the beta frequency (13-30 Hz) band. Using logistic regression models, we determined the combined and separate impacts of these factors on network entropy, a measure of the upper bound of information coding capacity. Importantly, changes in these features in dopamine-depleted rats led to a significant decrease in GPe network entropy. Changes in firing rates had the largest impact on entropy, with changes in synchrony also decreasing entropy at the network level. Changes in autocorrelations tended to offset these effects because autocorrelations decreased entropy more in the control animals. Thus it is possible that reduced information coding capacity within basal ganglia networks may contribute to the behavioral deficits accompanying PD.

Show MeSH
Related in: MedlinePlus