Effects of unilateral frontal eye-field lesions on eye-head coordination in monkey.

We studied the effects of unilateral frontal eye-field (FEF) lesions on eye-head coordination in monkeys that were trained to perform a visual search task. Eye and head movements were recorded with the scleral search coil technique using phase angle detection in a homogeneous electromagnetic field. In the visual search task all three animals showed a neglect for stimuli presented in the field contralateral to the lesion. In two animals the neglect disappeared within 2-3 wk. One animal had a lasting deficit. We found that FEF lesions that are restricted to area 8 cause only temporary deficits in eye and head movements. Up to a week after the lesion the animals had a strong preference to direct gaze and head to the side ipsilateral to the lesion. Animals tracked objects in contralateral space with combined eye and head movements, but failed to do this with the eyes alone. It was found that within a few days after the lesion, eye and head movements in the direction of the target were initiated, but they were inadequate and had long latencies. Within 1 wk latencies had regained preoperative values. Parallel with the recovery on the behavioral task, head movements became more prominent than before the lesion. Four weeks after the lesion, peak velocity of the head movement had increased by a factor of two, whereas the duration showed a twofold decrease compared with head movements before the lesion. No effects were seen on the duration and peak velocity of gaze. After the recovery on the behavioral task had stabilized, a relative neglect in the hemifield contralateral to the lesion could still be demonstrated by simultaneously presenting two stimuli in the left and right visual hemifields. The neglect is not due to a sensory deficit, but to a disorder of programming. The recovery from unilateral neglect after a FEF lesion is the result of a different orienting behavior, in which head movements become more important. It is concluded that the FEF plays an important role in the organization and coordination of eye and head movements and that lesions of this area result in subtle but permanent changes in eye-head coordination.