The role of the intermediate and deep layers of the superior colliculus in the control of posture and movement in the nonhuman primate

Abstract

The intermediate and deep layers of the superior colliculus (DLSC) represent a principle target of basal ganglia output via the nigrotectal pathway from the substantia nigra pars reticulata (SNpr). In the nonhuman primate, unilateral inhibition of SNpr with the GABA-A agonist muscimol (MUS) elicits abnormal postures and motor movements including dystonic head tilt (torticollis), body lean/ twist (postural asymmetry), quadrupedal rotations and dyskinesias. Some of these abnormalities can also be elicited by disinhibition of DLSC with the GABA-A antagonist bicuculline methiodide. Here I investigated whether DLSC mediates abnormal motor and posture evoked from SNpr in the nonhuman primate. I pre-treated the DLSC with MUS to prevent nigra-evoked disinhibition and examined the behavioral response to intranigral MUS. Control infusions contained saline in the same volume. Intracerebral drug infusions were done by removable cannulae inserted via an infusion grid positioned within a stereotaxically implanted chamber. To investigate whether DLSC mediates nigra-evoked head tilt and body lean/twist, bilateral, ipsilateral or contralateral infusions of MUS (9 nmol) in DLSC were followed by unilateral infusion of MUS (9 nmol) into either the left or right SNpr. The pre-treatments with MUS in DLSC prevented or reduced the expression of the head tilt in all 4 animals and prevented or reduced the expression of the accompanying body lean/twist in 3 of the 4 animals. Bilateral pre-treatment was used to investigate the role of DLSC in the nigra-evoked quadrupedal rotations which were evoked in 2 of the 4 animals. Bilateral pre-treatment with MUS in DLSC did not reduce the rate of the quadrupedal rotations but altered the posture in one of the animals. In this animal, MUS pre-treatment in DLSC prevented the accompanying head turning and resulted in quadrupedal rotations that were wider in radius. The study suggests that DLSC activity is necessary for the nigra-evoked head tilt, body lean/twist and head turning but not quadrupedal rotations. The results also demonstrate that the normal state of the nigrotectal pathway (DLSC is normally under tonic inhibition by SNpr) is important in maintaining normal posture and motor movements.