Neural maps of head movement vector and speed in the optic tectum of the barn owl

Abstract

1. This study investigates the contribution of the optic tectum in encoding the metric and kinetic properties of saccadic head movements. We describe the dependence of head movement components (size, direction, and speed) on parameters of focal electrical stimulation of the barn owl's optic tectum. The results demonstrate that both the site and the amount of activity can influence head saccade metrics and kinetics. 2. Electrical stimulation of the owl's optic tectum elicited rapid head movements that closely resembled natural head movements made in response to auditory and visual stimuli. The kinetics of these movements were similar to those of saccadic eye movements in primates. 3. The metrics and kinetics of head movements evoked from any given site depended strongly on stimulus parameters. Movement duration increased with stimulus duration, as did movement size. Both the size and the maximum speed of the movement increased to a plateau value with current strength and pulse rate. Movement direction was independent of stimulus parameters. 4. The initial position of the head influenced the size, direction, and speed of movements evoked from any given site: when the owl initially faced away from the direction of the induced saccade, the movement was larger and faster than when the owl initially faced toward the direction of the induced movement. 5. A characteristic movement of particular size, direction, and speed could be defined for each site by the use of stimulation parameters that elicited plateau movements with normal kinetic profiles and by having the head initially centered on the body. The size, direction, and speed of these characteristic movements varied systematically with the site of stimulation across the tectum. The map of head movement vector (size and direction) was aligned with the sensory representations of visual and auditory space, such that the movement elicited from a given site when the owl initially faced straight ahead brought the owl to face that region of space represented by the sensory responses of the neurons at the site of stimulation. 6. The results imply that both the site and the amount of neural activity in the optic tectum contribute to encoding the metrics and kinetics of saccadic movements. A comparison of the present findings with previous studies on saccadic eye movements in primates and combined eye and head movements in cats suggests striking similarities in the ways in which tectal activity specifies a redirection in gaze to such dissimilar motor effectors as the eyes and head.