Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus

Abstract

Previous investigations of the effects of ablations of the primate superior colliculus have produced conflicting results: several studies reported deficits in the accuracy of visually guided saccades while others reported primarily deficits in the latency of visually guided saccades. The present experiments attempted to resolve this conflict by examining the effects of complete lesions of the superior colliculus on the initiation and accuracy of saccades to central and peripheral visual targets. Four rhesus monkeys were trained to make saccades to visual stimuli and were then given large unilateral surgical ablations of the superior colliculus. Histological reconstructions of the brain stems showed that colliculus removal in all 4 monkeys was nearly complete and included the superficial and deep layers, representing the central and peripheral portions of the visual field. However, in 3 monkeys the lesions also included extensive regions anterior to the colliculus in the pretectum and in the posterior-medial thalamus. After the ablations the 3 monkeys with more extensive lesions showed a long-lasting deficit in the ability to make accurate saccades from a central fixation point to eccentric visual targets on the side contralateral to the ablation. Saccades to targets > .apprx. 20.degree. from the central fixation point consistently fell short and were not corrected by subsequent saccades. In the 4th monkey, with the ablation nearly restricted to the colliculus, deficits in the accuracy of initial saccades to visual targets on the side contralateral to the lesion were relatively small and were readily corrected by 2nd saccades. Monkeys were then tested to determine whether the deficits in the accuracy of saccades were related to the amplitude of the saccades or to saccades make to peripheral eye positions. The monkeys were required to make the same-amplitude saccades but from fixation points of varying eccentricity. After the ablations, the error in eye position for saccades to visual targets increased with the eccentricity of the target. Fixations of peripheral targets on the contralateral side were also in error. Errors in fixation and saccades were proportional to the eccentricity of the visual target. The oculomotor deficit was not specifically related to the amplitude of the saccade but rather to the position of the eye in the orbit. While only 3 of the 4 monkeys demonstrated deficits in achieving eccentric eye positions, all 4 monkeys demonstrated increased latencies for saccades to targets throughout the visual field contralateral to the ablation. Latency deficits were not correlated with eye position and largely recovered during the 1st mo. of testing. The effect of complete unilateral ablation of the superior colliculus alone produces only minimal effects on the initiation and accuracy of saccades. When there is additional damage to the pretectum and posterior-medial thalamus, severe and long-lasting deficits in accuracy are produced. The deficit appears to be an inability to match accurately the position of the eye to visual targets. The nuclei in the pretectum and posterior-medial thalamus may be the critical structures in producing this deficit, possibly because of their interconnections with the superior colliculi and frontal eye fields. These observations are consistent with a model of oculomotor control that assumes that a visually guided saccade is generated using a signal specifying the position of the target in space.