Oscillators and Oscillations in the Basal Ganglia

What is the meaning of an action potential? There must be different answers for neurons that fire spontaneously, even in the absence of synaptic input, and those driven to fire from a resting membrane potential. In spontaneously firing neurons, the occurrence of the next action potential is guaranteed; only variations in its timing can carry the message. In the basal ganglia, the globus pallidus, the substantia nigra, and the subthalamic nucleus consist of neurons firing spontaneously. They each receive thousands of synaptic inputs, but these are not required to maintain their background firing. Instead, synaptic interactions among basal ganglia nuclei comprise a system of coupled oscillators that produces a complex resting pattern of activity. Normally, this pattern is highly irregular and uncorrelated, so that the firing of each cell is statistically independent of the others. This maximizes the potential information that may be transmitted by the basal ganglia to its target structures. In Parkinson’s disease, the resting pattern of activity is dominated by a slow oscillation shared by nearly all of the neurons. Treatment with deep brain stimulation may gain its therapeutic value by disrupting this shared pathological oscillation, and restoring independent action by each neuron in the network.

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