Deficits of smooth pursuit eye movements after frontal and parietal lesions

To assess the contribution of the human frontal and parietal cortices to smooth pursuit (SP) eye movements, we recorded ocular motor responses to predictable (periodic) and unpredictable (step-ramp) foveal pursuit stimuli and to constant-velocity optokinetic full-field motion in 31 patients with chronic focal unilateral hemispheric lesions and in 50 age-related healthy adults, using infrared reflection oculography. Lesions were located either in the posterior parietal cortex (PPC), leaving the visual fields largely intact, or in the region of the frontal eye fields (FEF), the dorsolateral prefrontal cortex (PFC) or the supplementary motor area (SMA). We found (i) directional deficits in terms of lower pursuit velocities with ipsiversive target motion, more pronounced with predictable than with step-ramp stimuli, in patients with FEF lesions more frequently (in each of the four cases) than in patients with PPC lesions (in four out of 13 cases with foveal and in eight out of 13 cases with optokinetic stimulation); (ii) a relatively prolonged latency of direction reversal with periodic constant-velocity stimuli after SMA lesions (three cases), implying impaired anticipation of the target trajectory; (iii) no SP deficits following selective prefrontal lesions (eight cases); (iv) in some patients with PPC lesions (four out of 13) retinotopic deficits of SP initiation in both horizontal directions when step-ramp stimuli started in the contralesional hemifield, including prolonged pursuit latencies, which were independent of contralateral visual hemineglect. Directional and retinotopic SP deficits in patients with PPC lesions corresponded to SP deficits after unilateral lesions of middle temporal (MT) and medial superior temporal (MST) cortex in the monkey, and occurred only when lesions included the junction of Brodmann areas 19, 37 and 39, where the human homologues of MT and MST are assumed to lie. In conclusion, human SP eye movements are controlled, as in non-human primates, by a network of frontal and posterior cortical areas. Selective damage to each of these areas impairs specific SP subfunctions, reflecting subsequent stages of cortical processing from visual motion input to SP-related motor output.