David P. Carey

Do action systems resist visual illusions

Arguments about the relative independence of visual modules in the primate brain are not new. Recently, though, these debates have resurfaced in the form of arguments about the extent to which visuomotor reaching and grasping systems are insensitive to visual illusions that dramatically bias visual perception. The first wave of studies of illusory effects on perception and action have supported the idea of independence of motor systems, but recent findings have been more critical. In this article, I review several of these studies, most of which (but not all) can be reconciled with the two-visual-systems model.

Eye–hand coordination: Eye to hand or hand to eye?

Single-unit recording has revealed both hand and eye movement-related activity in the parietal cortex of the macaque monkey. These experiments, as well as neuropsychological studies, are unravelling the complex nature of how the eye and the hand work together in the control of visually guided movements.

The perception and prehension of objects oriented in the depth plane

Previous studies have reported that the visual form agnosic D.F. is able to use information about visual targets for the control of motor acts, but has great difficulty in using the same visual information for perceptual report. This intact visuomotor performance may be mediated by relatively intact parieto-frontal cortical mechanisms. The present study investigated the ability of D.F. to use binocular and monocular information about the orientation of an object in the depth plane for perceptual and visuomotor purposes. A square plaque was presented at seven different orientations in depth to D.F. and to three age- and sex-matched control subjects. Subjects were required to reach out and grasp the plaque using a precision grip (index finger and thumb) under binocular and monocular viewing conditions, and in separate trials to match the orientation of a hand-held plaque to the perceived orientation of the target object, also under both binocular and monocular conditions. D.F.s performance in grasping trials was found to be normal under binocular conditions, but was substantially worsened by removal of binocular vision. She was severely impaired at matching the orientation of the test square, although under binocular conditions her performance rose clearly above chance. The data suggest that the separation of cortical processing for visuomotor and visual perceptual purposes also applies, at least in part, to information about the orientation in depth of an object. The impaired performance under monocular viewing conditions on the visuomotor task is in agreement with recent physiological data and suggests that posterior parietal systems depend critically on binocular input for the processing of orientation in depth when ventral-stream information is unavailable.

Perception and Action in Depth

Little is known about distance processing in patients with posterior brain damage. Although many investigators have claimed that distance estimates are normal or abnormal in some of these patients, many of these observations were made informally and the examiners often asked for relative, and not absolute, distance estimates. The present investigation served two purposes. First, we wanted to contrast the use of distance information in peripersonal space for perceptual report as opposed to visuomotor control in our visual form agnosic patient, DF. Second, we wanted to see to what extent her abilities to process distance cues were dependent on binocular vision, in light of Milner et al.s (1991) observations of preserved stereopsis in DF, and Dijkerman et al.s (1996) and Marotta et al.s (1997) observations that her visual guidance of grasping may be particularly dependent on binocular vision of the target. We hypothesized that DFs visuomotor responses would show normal sensitivity to target distance, while her perceptual estimates would not. In the first experiment, we required DF and two age- and sex-matched control subjects to reach out and grasp black cubes placed at varying distances, or to estimate the distance of the cubes from the hand starting position without making a reaching movement. In the second experiment, we required DF and two age-matched control subjects to point as rapidly and accurately as possible to small LED targets which differed in spatial location, under binocular and monocular conditions. The results showed that, relative to the control subjects, DFs grasping movements produced normal peak velocity-distance scaling-when she reached for blocks which varied in depth or pointed to LED targets which were presented at different distances in depth. In contrast, in the cube experiment, her verbal estimates of object distance were poorly scaled, although they improved slightly under the binocular conditions. The results are discussed in terms of current theories of processing streams in extrastriate visual cortex and the distinction between categorical and coordinate spatial processing.

Hemispatial differences in visually guided aiming are neither hemispatial nor visual

Many studies have found differences in movements made to either side of the body midline. A popular interpretation of these differences has been that movements made by the arm, which is on same side of space in which the visual target appeared, are faster and better organised because they are processed within-hemisphere. Carey et al. (Experimental Brain Research 112 (1996) 496) showed that hemispatial movement differences cannot be accounted for by such a model. Their data suggested that biomechanical factors such as those proposed by Gordon et al. (Experimental Brain Research 99 (1994) 112) could better account for differences in movement duration and several characteristics of velocity and acceleration. The present study examines these arguments by requiring subjects to make rapid pointing movements in two experiments. In the first, results demonstrated that hemispatial effects occurred in pointing movements made without any visual target or vision of the limb. These findings suggest that intra- and inter-hemispheric models are untenable. Gordon et al. argued that hand path direction relative to the long axis of the upper arm accounts for hemispatial effects on kinematics. In the second experiment hand path direction and hemispace were dissociated. Contralateral movements were performed more efficiently than ipsilateral movements, when target and starting positions required an adductive movement to acquire the contralateral target and an abductive movement to acquire the ipsilateral target. These results provide strong support for the Gordon et al. model, although the possible contributions of other dynamic factors and/or differential control of proximal and distal muscles by the central nervous system cannot be ruled out.

Tapping, grasping and aiming in ideomotor apraxia

Very few studies have investigated sensorimotor control in apraxia using tasks that differ in movement complexity. Nevertheless, there is some evidence to suggest that spontaneous behaviour, although relatively preserved, can be rather clumsy or awkward, and that patients with ideomotor apraxia may have subtle kinematic abnormalities in movements made in the laboratory. It remains unclear whether patients with ideomotor apraxia perform normally on movements such as visually guided aiming, that may not depend on higher-order, more cognitive, processes and that are relatively unguided by overlearned contexts. In this study, three different sensorimotor tasks were given to the same sample of patients with quantified apraxic disturbance. Finger tapping, goal-directed grasping and aiming with and without visual feedback were examined in these patients. A clear dissociation was found between grossly impaired gesture imitation and intact motor programming of goal-directed movements with visual feedback. Apraxic patients were, however, impaired on aiming movements without visual feedback, suggesting that apraxia is associated with an increased reliance on integration of online visual information with feedforward/feedback somatosensory and motor signals. Furthermore, patients were impaired on single finger tapping which was a surprisingly good predictor of apraxia severity.

Asymmetries in Motor Attention during a Cued Bimanual Reaching Task: Left and Right Handers Compared

Several studies have indicated that right handers have attention biased toward their right hand during bimanual coordination (Buckingham and Carey, 2009; Peters, 1981). To determine if this behavioral asymmetry was linked to cerebral lateralization, we examined this bias in left and right handers by combining a discontinuous double-step reaching task with a Posner-style hand cueing paradigm. Left and right handed participants received a tactile cue (valid on 80% of trials) prior to a bimanual reach to target pairs. Right handers took longer to inhibit their right hand and made more right hand errors, suggesting that their dominant hand was more readily primed to move than their non-dominant hand, likely due to the aforementioned attentional bias. Left handers, however, showed neither of these asymmetries, suggesting that they lack an equivalent dominant hand attentional bias. The findings are discussed in relation to recent unimanual handedness tasks in right and left handers, and the lateralization of systems for speech, language and motor attention.

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

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 DFs 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.

Neuropsychological perspectives on eye-hand coordination in visually-guided reaching

Substantial progress has been made in understanding the neural control of movement in the past 30 years. Lower cost technology for tracking movements of the eyes and the hands has increased our understanding of these two systems and their interactions in both neurologically intact individuals and non-human primates. Nevertheless the neuropsychology of eye-hand coordination during visually-guided tasks such as reaching and grasping remains relatively understudied. This chapter reviews some of the relevant neurophysiology and neuropsychology of eye-hand coordination during visually-guided reaching. Current models emphasising coordinate transformations are discussed in light of new patient data showing a particular type of failure of eye-hand coordination during reaching.

Memory-driven movements in limb apraxia: is there evidence for impaired communication between the dorsal and the ventral streams?

Memory-driven reaching and grasping movements were analysed in patients with left cerebral hemispheric damage and impaired gesture imitation. The dorsal and ventral streams of the visual pathway model of Milner and Goodale (Milner and Goodale, The Visual Brain in Action, 1995) are thought to operate relatively independently. However, cross-connections between the areas of each pathway are likely to enable interactions essential for higher-level praxis. Apraxic errors such as seen in gesture imitation can possibly be understood as arising from a disconnection of the two visual pathways. If the integrated action of the perceptual and visuomotor systems in patients with apraxia is compromised, then we would expect to find indications of impaired motor programming and misreaching in these patients when making movements driven by stored representations. Such a pattern, however, was not found in our sample of apraxic patients. Patients with limb apraxia produced normal movement kinematics and normal end-point accuracy when making memory-driven reaching movements with or without visual guidance of movement. Furthermore, perceptual information about object size and object distance were incorporated as normal in memory-driven grasping movements of these patients.