Motion parallax enables depth processing for action in a visual form agnosic when binocular vision is unavailable

Abstract

Visual-form agnosic patient DF, who has severe difficulties in using visual information about size, shape and orientation for perceptual report, can nevertheless—under normal viewing conditions—use the same information to accurately guide her hand movements. However, her performance of prehension tasks requiring the analysis of visual depth is severely disrupted when binocular vision is prevented. We have suggested that this deterioration in visuomotor control is due to an inability to use pictorial depth cues to compensate for the removal of binocular vision. In the current study we investigated whether DF was able to use motion parallax as an alternative to binocular cues. We asked her to grasp a square plaque slanted at different orientations in depth, under two monocular testing conditions. In one condition her head remained stationary on a chin rest, and in the other condition she made large lateral head movements just prior to each prehension movement. The results confirmed that DF is impaired in adjusting her hand orientation to the orientation of the target object when reaching monocularly with her head stationary. In contrast, when she made head movements, her manual performance was restored to almost normal levels. Our results are consistent with the idea that the processing of pictorial depth cues depends on the cortical ventral stream, which is known to be disrupted by DF’s lesion. They further indicate that orientation in depth can be computed from motion parallax just as well as from binocular cues in the absence of a normally functioning ventral stream.

Introduction

There has been considerable progress in our understanding of the neural mechanisms underlying visuomotor function during the past 20 years. This research has led to the proposal that the visual areas constituting the ‘dorsal stream’, extending from V1 to the posterior parietal cortex, provide the default system for processing visual information for the on-line guidance of actions [6], [9]. This role contrasts with that of the ventral stream (terminating in the inferior temporal cortex) which is generally thought to lie in the mediation of visual perception and visual recognition.

The processing of visual depth must play an important role both in visuomotor control and in our perception of objects. However, the computation of depth may be achieved by means of different cues in the two cases. Previous investigations have shown that depth cues derived from binocular vision play an important role for the on-line control of movements. In normal subjects the accuracy and kinematic characteristics of movements made under monocular viewing conditions differ only slightly from those made under binocular viewing conditions [8], [23], presumably because the subjects can rely on various ‘pictorial’ cues available in the retinal array in both cases. But monocular occlusion can have much more dramatic effects on visuomotor control in certain brain damaged patients. This is true of the visual-form agnosic patient DF, who has severe difficulties in using visual information about size, form and orientation for perceptual report, but who can under normal viewing conditions, guide her hand movements very accurately using that same visual information [7], [20]. DF’s ability to perform visuomotor tasks requiring depth processing becomes severely disrupted when binocular vision is prevented [1], [3], [12].

We have previously suggested that DF’s impaired visuomotor performance under these monocular viewing conditions is due to her inability to use pictorial depth cues to compensate for the loss of binocular vision [3]. Independent evidence for a reliance of the visuomotor system on pictorial depth cues during monocular viewing comes from studies with normal subjects. Marotta and colleagues [13] showed that grip aperture during reaching to grasp an object is more susceptible to pictorial size illusions under monocular viewing conditions than when binocular vision is available. Furthermore, Marotta and Goodale [14] demonstrated that normal subjects can use a learned relationship between a pictorial cue (elevation of the object in the visual scene) and target distance for the programming of grasping movements under monocular viewing conditions.

Milner and colleagues [19], [20] have argued that the presence of dense bilateral damage to lateral prestriate areas in DF has caused a disconnection of V1 from the pattern processing systems in inferior temporal cortex. Good evidence for this interpretation has recently come from a functional MRI study which found that the activation seen in these temporal-lobe areas when healthy subjects view pictures of everyday objects was absent in DF, despite a normal pattern of activation in her primary visual area V1 (T. James and M.A. Goodale, personal communication). Since it would be reasonable to assume that an intact ventral stream is required for the processing of pictorial depth cues, damage to this system in DF would be expected to cause an abnormal dependence upon non-pictorial cues, such as those provided by binocular disparity.

Another possible non-pictorial source of depth information, however, is the relative motion of stimuli on the retina that is generated by lateral head movements. Such ‘motion parallax’ information can provide relative depth information about the different elements in a display [22]. Investigations by Marotta and colleagues [16] suggest that monocularly enucleated patients use retinal motion cues created by spontaneous head movements in the control of prehension movements to compensate for their loss of binocular vision [16]. These authors have also found that normal subjects benefit from such head movements under impoverished visual conditions in which monocular viewing causes clear reductions in reaching efficiency [15]. The current study investigated whether patient DF was able to use motion parallax to compensate for the absence of binocular vision when performing the visuomotor act of grasping a square plaque slanted in depth. Lateral movements of the head would cause relative motion on the retina between the front and back edges of the plaque, thus generating parallax information about the plaque’s orientation.

On the assumption that DF’s lesion has mainly affected the ventral stream of visual processing, we have proposed that her visuomotor skills are mediated by the dorsal visual stream [19]. In the context of that proposal, the current experiment asks whether the dorsal stream is able to use motion parallax as an alternative non-pictorial depth cue when binocular disparity is unavailable.