Experiments in the 1980's established that the basal ganglia is critical to the expression of superior colliculus (SC)- mediated orientation behaviors. They physiology of the double inhibitory striato-nigro-tectal circuit mediating this interaction is well known: increased activity of striatal neurons suppresses the tonic inhibitory effects normally imposed by substantia nigra (SNr) neurons on SC tectospinal output neurons. The disinhibition of tectospinal neurons allows them to influence eye/head movements via their connections with regions of the brainstem and spinal cord. However, recent advances in unraveling the intrinsic circuitry of the basal ganglia have heightened our appreciation of the role played by inhibition in shaping motor behaviors. This has provided impetus to the emerging idea that the essential contribution of the basal ganglia to motor behavior is to coordinate selections of desired responses among competing, and often conflicting, behavioral needs. Thus, while desired motor behaviors are to be engaged (by disinhibition), competing sensory and/or motor responses that might otherwise interfere with the intended movements must be prevented (by inhibition). Indeed, contemporary models of the limb movement control by the globus pallidus, pars interna (the functional homologue of the SNr for limb movements have incorporated both processes. Nevertheless, despite the obvious implications that such synergistic processes would have in transforming our current understanding of the SC, no effort has been made to integrate such concepts into models of SC-mediated behaviors. Based on our observations made in the previous grant period, we propose a model wherein the basal ganglia uses three distinct populations of nigrotectal neurons, coupling focal disinhibition with widespread inhibition tot modulate SC activity. These influences are exerted via crossed and uncrossed nigrotectal neurons to coordinate activity in the colliculi on both sides of the brain. Specifically, phasic inhibition of GABAergic nigrotectal neurons in the ipsilateral SNr produces disinhibition of tectospinal neurons in the ipsilateral 'saccade zone' that specify the metrics of the desired eye/head movements. At the same time, phasic activation of GABAergic nigrotectal neurons in the rostral aspect of the same SNr inhibits both ipsilateral fixation neurons (to disengage fixation) and contralateral saccade neurons (that might initiate opposing movements). Thus, competing sensory stimuli and/or motor events are prevented from gaining access to the brainstem circuitry that could impair the accuracy of the specified movement. Experiments to test the predictions of this model will provide insights into the interplay that exists between cortical and subcortical structures and how such activity is coordinated by the basal ganglia.
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