Subcortical contributions to head movements in macaques. I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus

Abstract

1. These studies were initiated to understand the neural sites and mechanisms controlling head movements during gaze shifts. Gaze shifts are made by saccadic eye movements with and without head movements. Sites were stimulated electrically within the brain stem of awake, trained monkeys relatively free to make head movements to study the head-movement components of gaze shifts. 2. Electrical stimulation in and around the gigantocellular reticular nucleus evoked head movements in the ipsilateral direction. Gaze shifts were never evoked from these sites, presumably because the vestibulo-ocular reflex compensated. The rough topography of this region included large head movements laterally, small movements medially, downward movements from dorsal sites, and upward movements more ventrally. 3. The initial position of the head influenced the magnitude of the elicited movement with larger movements produced when the head was directed to the contralateral side. Attentive fixation was associated with larger and faster head movements when compared with those evoked during spontaneous behavior. 4. The superior colliculus makes a significant contribution to gaze shifts and has been shown to contribute to head movements. Because the colliculus is a major source of afferents to the gigantocellular reticular nucleus, comparable stimulation studies of the superior colliculus were conducted. When the colliculus was excited, shifts of gaze in the contralateral direction were predominant. These were most often accomplished by saccadic eye movements, however, we frequently elicited head movements that had an average latency 10 ms longer than those elicited from the reticular head movement region. Sites evoking head movements tended to be deeper and more caudal than loci eliciting eye movements. Neither the onset latencies, amplitudes, nor peak velocities of head movements and eye movements were correlated. Gaze shifts evoked from the caudal colliculus with the head free were larger than those elicited from the same site with the head fixed. 5. These studies demonstrate that both the superior colliculus and gigantocellular reticular nucleus mediate head movements. The colliculus plays a role in orienting to external events, and so collicular head movements predominantly were associated with gaze shifts, with the eye and head movements uncoupled. The medullary reticular system may play a role in the integration of a wider range of movements. Head movements from the medullary reticular sites probably participate in several forms of head movements, such as those that are related to postural reflexes, started volitionally, and/or oriented to external events.