We investigated smooth pursuit eye movements in 72 patients with focal cerebral lesions using a sinusoidal pursuit task at multiple target frequencies and amplitudes. Twenty patients had normal pursuit gain and symmetry at all target frequencies, 12 had strictly ipsilesional pursuit deficit, 19 had symmetric bi-directional pursuit deficit, 18 had asymmetric bi-directional pursuit deficit (the deficit being more severe on the side of the lesion) and three had more severe contra-directional deficit. Normal pursuit gain was found in patients whose lesions were limited to the frontal, temporal and occipital poles, or the primary somaesthetic areas. Predominant ipsilesional pursuit deficit occurred in a long band of lesion overlap areas that run from the V5 occipito-temporal areas posteriorly, through the internal sagittal stratum, the posterior and anterior limbs of the internal capsule with adjacent striatum, to the dorsomedial frontal cortex anteriorly. Symmetric bi-directional deficit was associated with lesions involving the regions of the cortico-limbic-reticular network for directed attention, including the frontal eye fields, the posterior parietal cortex and the thalamus. Asymmetric bi-directional deficit resulted from lesions that penetrated into the underlying/adjacent white matter from the frontal eye field, posterior parietal cortex and thalamus. Varying combinations of lesions in the areas associated with uni-directional and symmetric bi-directional deficits produced a graded continuum from strict ipsi-directional pursuit deficit, through asymmetric bi-directional deficit, to symmetric bi-directional deficit. The striatum was identified as the area of lesion overlap in patients with large phase errors. Patients with lesions involving the right posterior parietal cortex and/or right dorsolateral frontal cortex had significantly more severe impairments than their counterparts with left-sided lesions. All pursuit deficits were more pronounced at high frequencies.