While accumulating evidence now supports the notion that several anatomical targets of the basal ganglia play a critical role in eye movement generation by making decisions both about what movement to make and when to make those movements, studies in the basal ganglia are beginning to suggest a different role for these nuclei. Several lines of research now suggest that the basal ganglia play an evaluative role, assessing whether recently completed movements were of value to an organism. If this is true, then movement disorders associated with basal ganglia dysfunction must be viewed as fundamentally different from movement disorders associated with damage to areas involved in movement execution. A series of experiments are proposed to test this hypothesis. First, the proposal attempts to determine whether eye movement-related neurons in the substantia nigra pars compacta signal when an unexpectedly positive outcome has occurred, when an unexpected reward has been obtained by the organism. Second, the proposal attempts to test the hypothesis that caudate neurons use this information to determine what specific movements may have led to the unexpectedly positive outcome. Three sets of experiments engage these two hypotheses: i) Do neurons of the pars compacta encode the time and value of an unexpected reward (as quantitatively predicted by theories of reinforcement learning) but do not carry information about the metrical properties of recent movements? A set of single-unit recording studies, driven by existing theoretical models, engage this question, ii) Do saccade-related neurons in the caudate nucleus carry a signal that determines which eye movements account for the unexpected rewards signaled by compacta activity? A set of single-unit recording studies driven by recent results in the caudate engage this question. iii) Does artificial activation of compacta cause the caudate to produce new links between movements and rewards, and if so what is the temporal signature of this attributional process? A combination of single-unit recording and microstimulation techniques seek to causally link compacta activation to both behavioral responses and caudate activity patterns. Together these experiments would help provide a new circuit-level overview of the function of the basal ganglia, an overview which would have a significant impact on both future basic research and clinical models of basal ganglia function in eye movement control.
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