Neuronal networks for control of eye movement

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Our current research is focused on the neuronal networks in the basal ganglia which control eye movements. We have shown that sensory and cognitive signals carried by neurons in the basal ganglia are strongly modified by expected reward. We hypothesized that the reward-dependent modulation occurs within the basal ganglia. Specifically, excitatory inputs from the cerebral cortical areas to the caudate nucleus (CD), which carry spatial signals, are modulated by inputs from midbrain dopamine (DA) neurons. To test this model, we conducted two kinds of experiments as shown below. DA antagonist injections: A brain area called the basal ganglia is known to contain neurons (nerve cells) that control voluntary initiation of body movements. Here we show that the normal release of a neurotransmitter, called dopamine, in the basal ganglia is necessary for orienting eyes to something rewarding. We injected a small amount of drugs that prevent dopamine from binding to its receptors on neurons in the caudate nucleus, part of the basal ganglia, while animals were orienting their eyes to a light spot associated with a large reward or to another spot associated with a small reward. One drug, called D1 antagonist, slowed eye movements to a large reward-associated spot, while another drug, called D2 antagonist, slowed eye movements to a small reward-associated spot. Our study demonstrates that complex neural circuits, acting as a movement controller, are fine-tuned by a specific chemical substance, dopamine, to achieve goals that are critical for survival. Comparison between the basal ganglia and the cerebral frontal cortex: We report that single neuron activity in the cortex and basal ganglia, two higher-order areas controlling movement generation, reflects preference for larger reward. In the non-human primate model system using eye movement, it has been generally assumed that the frontal eye field (a cortical area) specifies movement metrics (e.g., direction, amplitude), while the basal ganglia provides motivational information (e.g., whether a movement will result in reward). Here we show that, using the same monkeys in the same task, expected reward modulates single neuron activity in both the frontal eye field and basal ganglia, if such activity also carries movement metrics-related information. These results raise the possibility that cortex may also contribute motivational information to reward modulated behaviors. Further elucidation of the origin and function of the motivation information in the cortex might lead to identification of new neural targets for compensating motivation-related deficits in patients with compromised basal ganglia functions.