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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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Decrease in entropy (ΔH) as function of ensemble size and model prediction. A: average ΔH in 400 random ensembles of simultaneously recorded neurons of each size (thin lines; error bars are ±SE) and model predictions (thick lines). B: predicted ΔH as a function of ensemble size for large populations.
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f7: Decrease in entropy (ΔH) as function of ensemble size and model prediction. A: average ΔH in 400 random ensembles of simultaneously recorded neurons of each size (thin lines; error bars are ±SE) and model predictions (thick lines). B: predicted ΔH as a function of ensemble size for large populations.

Mentions: We carried out this analysis in two steps. First, we showed that our model predicted correlation values in small ensembles of ≤12 simultaneously recorded neurons (Fig. 7A). Although we had a few larger ensembles, we were not able to subsample enough different ensembles of >12 neurons to derive reliable estimates. We randomly selected 400 recorded ensembles of various sizes and calculated the change (decrease) in entropy (ΔH) as a function of ensemble size. We used our model to predict average ΔH values using information about pairwise correlations between recorded neurons. We found a close correspondence between our model and the data (Fig. 7A). Thus for small ensembles, our model closely predicted ΔH.


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)

Decrease in entropy (ΔH) as function of ensemble size and model prediction. A: average ΔH in 400 random ensembles of simultaneously recorded neurons of each size (thin lines; error bars are ±SE) and model predictions (thick lines). B: predicted ΔH as a function of ensemble size for large populations.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f7: Decrease in entropy (ΔH) as function of ensemble size and model prediction. A: average ΔH in 400 random ensembles of simultaneously recorded neurons of each size (thin lines; error bars are ±SE) and model predictions (thick lines). B: predicted ΔH as a function of ensemble size for large populations.
Mentions: We carried out this analysis in two steps. First, we showed that our model predicted correlation values in small ensembles of ≤12 simultaneously recorded neurons (Fig. 7A). Although we had a few larger ensembles, we were not able to subsample enough different ensembles of >12 neurons to derive reliable estimates. We randomly selected 400 recorded ensembles of various sizes and calculated the change (decrease) in entropy (ΔH) as a function of ensemble size. We used our model to predict average ΔH values using information about pairwise correlations between recorded neurons. We found a close correspondence between our model and the data (Fig. 7A). Thus for small ensembles, our model closely predicted ΔH.

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