Motion discrimination in cortically blind patients

Brain (2001), 124, 30–46 Motion discrimination in cortically blind patients Paul Azzopardi and Alan Cowey Department of Experimental Psychology, University of Oxford, Oxford, UK Correspondence to: Dr Paul Azzopardi, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK E-mail: Summary Some patients with brain damage affecting the striate cortex, though clinically blind in their field defects, can still discriminate visual stimuli when forced choice procedures are used. Such patients seem particularly sensitive to moving stimuli in their scotomata, though there are conflicting reports as to whether they can discriminate the direction of motion. We tested three patients with areas of cortical blindness for their ability to detect and discriminate the direction of motion of a variety of first-order motion stimuli, namely bars, gratings, plaids and random dot kinematograms depicting translation and motion in depth, during forced choice tasks. The patients could detect the presence of movement in any kind of stimulus, and could discriminate the direction of single bars, but none could discriminate the direction of motion of the more complex stimuli (gratings, plaids and random dot kinematograms) or discriminate between 0 and 100% coherent random dot kinematograms at any speed tested (from 4 to 64°/s). Similar results were obtained from one of the patients who was additionally tested with second-order versions of the translated bar and random dot kinematograms, eliminating light scatter as an explanation. Overall, the results suggest that motion processing in the scotoma is severely impaired, and that the puzzling discrepancies between previous studies can be accounted for by the type of stimulus used. The motion discrimination impairment caused by brain damage affecting the primary visual cortex is inconsistent with the proposed existence of a subcortical pathway to extrastriate cortical motion areas (such as areas MT and MST) which bypasses the striate cortex and is specialized for analysing ‘fast’ motion. Keywords: blindsight; visual motion perception; area V1; area V5/MT; superior colliculus Introduction The striate cortex (area V1) contains a topographic map of the visual field, such that locally damaging or disconnecting it causes blindness in the corresponding part of the visual field (Holmes, 1945). Some patients with a damaged striate cortex, though clinically blind as defined by perimetry, can detect and even discriminate between stimuli presented in their field defects when forced choice procedures are used, even though they deny seeing them (Pöppel et al., 1973; Weiskrantz et al., 1974). This phenomenon is known as blindsight. The range of visual capacities spared following striate cortex lesions includes the ability to locate and discriminate high-contrast targets by eye movements, by pointing and by verbal report (for reviews, see Weiskrantz, 1990; Stoerig and Cowey, 1997). Evidence from monkeys with striate cortex lesions and from brain-damaged patients suggests that these capacities are mediated by neural projections from the retina to the extrastriate visual cortex that bypass the predominant route from the retina to the striate cortex via the lateral geniculate nucleus, and which involve the superior colliculus and the lateral geniculate and pulvinar nuclei of the thalamus (Mohler and Wurtz, 1977; © Oxford University Press 2001 Rodman et al., 1989, 1990; Gross, 1991; Cowey and Stoerig, 1991; Bullier et al., 1994; King et al., 1996; Azzopardi et al., 1996). Moving stimuli are usually more readily detected in the field defects of cortically blind patients than static ones. In fact, moving targets may be so salient that, in carefully controlled conditions, it can be difficult to discern whether the patients are actually ‘blind’ to them (Riddoch, 1917; Holmes, 1918; Weiskrantz, 1990; Weiskrantz et al., 1995; Azzopardi and Cowey, 1998; Zeki and ffytche, 1998). Whether this reflects sensitivity to motion is open to question, for two reasons. First, moving stimuli have not always been equated for detectability with stationary stimuli in normal vision, i.e. moving targets could be detectable in the field defect because they are more easily detected than static targets in normal vision. Secondly, motion may be confounded with position and temporal frequency, both of which can be discriminated in the field defect independently of motion (Pöppel et al., 1973; Barbur et al., 1994). Several studies report that cortically blind patients can discriminate explicitly the direction of a variety of moving stimuli, including single Motion discrimination in blindsight spots (Blythe et al., 1986, 1987; Weiskrantz et al., 1995; King et al., 1996), bars (Barbur et al., 1993), gratings and plaids (Perenin, 1991; Benson et al., 1998; Morland et al., 1999), and random dot kinematograms depicting translation (Perenin, 1991; Benson et al., 1998; Zeki and ffytche, 1998) or motion in depth (Mestre et al., 1992). But others have found them unable to discriminate the direction of motion of gratings and random dot kinematograms depicting translation, relative motion and motion in depth (King et al., 1996; Barton and Sharpe, 1997), and monkeys with striate cortex lesions cannot discriminate the direction of moving gratings presented in the scotoma (Weiskrantz, 1963). The idea that motion processing is preserved in the scotoma is bolstered by studies of the properties of neurones in extrastriate cortical visual areas in monkeys with striate cortex lesions, especially area V5/MT, which is specialized in its sensitivity to motion direction (Dubner and Zeki, 1971; Albright, 1984). Recording from this area, Rodman and colleagues found that the visual responses of single neurones with receptive fields in the scotoma were weaker and more variable than normal after surgical or reversible lesions, yet about half of the neurones sampled still retained the ability to discriminate the direction of motion of bars swept through their receptive fields (Rodman et al., 1989). This finding was confirmed, and extended to include area V3a (another visual area specialized for motion), by Girard and colleagues (Girard et al., 1991, 1992). These were unexpected findings, given that few neurones in the superior colliculus, upon which residual motion sensitivity in area MT depends (Rodman et al., 1990), are directionally selective (Goldberg and Wurtz, 1972), and Gross (1991) therefore suggested that neurones in area MT must be able to compute directionality locally on the basis of non-directional information supplied by neurones in the superior colliculus. Given the evidence from single-unit recordings, it would be tempting to ignore those studies which did not find cortically blind patients able to discriminate direction of motion in the scotoma. A recent development, however, is the finding that neurones in cortical areas MT and MST of monkeys with long-stan (...truncated)