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The Journal of Neuroscience, December 13, 2006, 26(50):12921-12942; doi:10.1523/JNEUROSCI.3486-06.2006

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Behavioral/Systems/Cognitive
A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia

Mark D. Humphries, Robert D. Stewart, and Kevin N. Gurney

Adaptive Behaviour Research Group, Department of Psychology, University of Sheffield, Sheffield, S10 2TP, United Kingdom

Correspondence should be addressed to K. Gurney, Adaptive Behaviour Research Group, Department of Psychology, University of Sheffield, Sheffield, S10 2TP, UK. Email: k.gurney{at}shef.ac.uk

The basal ganglia (BG) have long been implicated in both motor function and dysfunction. It has been proposed that the BG form a centralized action selection circuit, resolving conflict between multiple neural systems competing for access to the final common motor pathway. We present a new spiking neuron model of the BG circuitry to test this proposal, incorporating all major features and many physiologically plausible details. We include the following: effects of dopamine in the subthalamic nucleus (STN) and globus pallidus (GP), transmission delays between neurons, and specific distributions of synaptic inputs over dendrites. All main parameters were derived from experimental studies. We find that the BG circuitry supports motor program selection and switching, which deteriorates under dopamine-depleted and dopamine-excessive conditions in a manner consistent with some pathologies associated with those dopamine states. We also validated the model against data describing oscillatory properties of BG. We find that the same model displayed detailed features of both -band (30–80 Hz) and slow (1 Hz) oscillatory phenomena reported by Brown et al. (2002) and Magill et al. (2001), respectively. Only the parameters required to mimic experimental conditions (e.g., anesthetic) or manipulations (e.g., lesions) were changed. From the results, we derive the following novel predictions about the STN–GP feedback loop: (1) the loop is functionally decoupled by tonic dopamine under normal conditions and recoupled by dopamine depletion; (2) the loop does not show pacemaking activity under normal conditions in vivo (but does after combined dopamine depletion and cortical lesion); (3) the loop has a resonant frequency in the -band.

Key words: neural network; action selection; dopamine; oscillations; subthalamic nucleus; globus pallidus

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Received Aug. 11, 2006; revised Oct. 11, 2006; accepted Oct. 28, 2006.

Correspondence should be addressed to K. Gurney, Adaptive Behaviour Research Group, Department of Psychology, University of Sheffield, Sheffield, S10 2TP, UK. Email: k.gurney{at}shef.ac.uk

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