Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events.

Abstract

The behavioral involvement of neurons in the pars reticulata of the substantia nigra (SNpr) in sensory and motor processes was investigated in order to contribute to the understanding of behavior-related neuronal mechanisms in the basal ganglia, of which the SNpr is a major output station. Electrophysiological properties of SNpr neurons were studied with extracellular recordings from single neurons in monkeys performing in a behavioral GO/NO-GO paradigm, employing significant auditory and visual stimuli, forelimb reaching movements, and mouth movements. Neurons in the SNpr discharged impulses of 0.6 to 1.0 ms in duration, at rates of 23 to 145/s (median 68/s). They contrasted with dopaminergic pars compacta neurons of substantia nigra, which discharged longer impulses at rates below 8/s. Two-thirds of more than 100 quantitatively and statistically evaluated SNpr neurons showed changes with temporal relationships to at least one of the events of the behavioral task. One-fifth of all neurons covaried with more than one event. The largest group of task-related neurons increased or decreased activity with contralateral forelimb movements (46% of all neurons). Most of them covaried with large forward reaching of the arm, and only the minority covaried with distal forearm manipulation. None of the SNpr neurons resembled in their changes the timing of activity of single muscles. Many neurons also showed changes with ipsilateral movements, in a similar fashion as on the contralateral side. Changes began rarely before and mostly with or after onset of muscle activity in prime movers. Changes were quantitatively moderate, rarely exceeding a doubling of discharge rate with increases and reductions by 50% with decreases. Movement relations did not appear to be due to somatosensory input. Some neurons increased or decreased their activity in relation to mouth movements (16% of all neurons). Changes were quantitatively moderate as in the case of movement relationships. Nine percent of all neurons decreased their activity after an acoustic preparatory signal and 9% after a light stimulus indicating the GO or NO-GO situation. Latencies were 50-150 ms (median 90 ms) for the auditory and 80-200 ms (median 120 ms) for the visual responses. Twelve percent of all neurons increased or decreased their activity during the waiting and preparation period, which lay between an initial sensory signal and the permission to move for reward.(ABSTRACT TRUNCATED AT 400 WORDS)