Cortical and tectal control of visual orientation in the gerbil: Evidence for parallel channels

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Abstract
Two experiments were carried out with Mongolian gerbils to determine the roles of optic tectum and visual cortex in the mediation of visually guided head turns and locomotion elicited and controlled by discrete visual targets. In Experiment 1, the behavior of animals with either a sham operation, a bilateral lesion of optic tectum, or a bilateral ablation of areas 17, 18a, and 18b was recorded on videotape as they ran from the center of a circular arena toward a small visual target projected in different locations around the perimeter of the arena. The amplitude and direction of the head turns and the accuracy of their locomotor responses were reconstructed from a frame by frame analysis of the videotapes. Sham-operate gerbils made a series of head turns before running accurately and efficiently toward the target. The gerbils with lesions of areas 17, 18a, and 18b rarely made more than one head turn before running toward the perimeter of the arena. Although the single head turn they did make was often well-correlated with the position of the target in their visual field, the direction of their locomotor response was largely determined by the direction and amplitude of that head turn. As a consequence, these animals undershot the target more often than did the sham-operate animals, and even ran into the visual half field opposite the target if their head turn had also been made into that half field. Unlike the sham operates, these animals were unable to make further adjustments in their orientation toward the stimulus after their initial head turn. The head turns and locomotor behavior of the gerbils with lesions of optic tectum were even more disorganized and inaccurate than those of the posterior decorticates. Nevertheless, when the target was presented within 45° from their visual midline, their head turns and locomotor responses showed a systematic relationship with the eccentricity of the target. Their behavior to stimuli outside this central wedge of their visual field was completely disorganized and showed no relationship to the location of the target. In Experiment 2, unilateral lesions of area 17 were performed in the gerbils that had already received bilateral tectal lesions to determine whether such lesions would affect the “residual” ability of these animals to orient toward stimuli located within the central portion of their visual field. During retesting, these animals were able to respond to targets only if they were located in the central portion of the field ipsilateral to the cortical lesion. These results suggest that orientation to discrete visual targets is mediated by both tectal and geniculostriate pathways with the tectofugal system subserving responses to stimuli throughout the entire visual field and the corticofugal system organizing behavior to stimuli within the central portion of the visual field. It is argued that the output from these two parallel sensorimotor systems converges on common motor centers in the pontine reticular formation.