Melvyn A. Goodale

Separate visual pathways for perception and action.

Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.

Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas

Although both reaching and grasping require transporting the hand to the object location, only grasping also requires processing of object shape, size and orientation to preshape the hand. Behavioural and neuropsychological evidence suggests that the object processing required for grasping relies on different neural substrates from those mediating object recognition. Specifically, whereas object recognition is believed to rely on structures in the ventral (occipitotemporal) stream, object grasping appears to rely on structures in the dorsal (occipitoparietal) stream. We used functional magnetic resonance imaging (fMRI) to determine whether grasping (compared to reaching) produced activation in dorsal areas, ventral areas, or both. We found greater activity for grasping than reaching in several regions, including anterior intraparietal (AIP) cortex. We also performed a standard object perception localizer (comparing intact vs. scrambled 2D object images) in the same subjects to identify the lateral occipital complex (LOC), a ventral stream area believed to play a critical role in object recognition. Although LOC was activated by the objects presented on both grasping and reaching trials, there was no greater activity for grasping compared to reaching. These results suggest that dorsal areas, including AIP, but not ventral areas such as LOC, play a fundamental role in computing object properties during grasping.

Visual control of reaching movements without vision of the limb

SummaryThe spatial and temporal organization of hand and eye movements were studied in normal human subjects as they pointed toward small visual targets. The experiment was designed to assess the role of information about target position in correcting the trajectory of the hand when view of the hand was not available. To accomplish this, the duration of target presentation was systematically varied across blocks of trials. The results of this experiment showed that pointing movements were about 3 times more accurate when the target was present throughout the entire pointing movement, than when the target disappeared shortly after the hand movement had begun. These data indicate that pointing movements made without view of the limb are not purely preprogrammed but instead, are corrected during their execution. These modifications to the motor program are smoothly integrated into the ongoing movement and must depend upon comparing visual information about the position of the target with non-visual information about the position of the limb. The source of this non-visual information was not directly established in the present experiment but presumably must be derived from kinesthetic reafferences and/or efference copy.

Factors affecting higher-order movement planning: a kinematic analysis of human prehension

SummaryPast studies of the kinematics of human prehension have shown that varying object size affects the maximum opening of the hand, while varying object distance affects the kinematic profile of the reaching limb. These data contributed to the formulation of a theory that the reaching and grasping components of human prehension reflect the output of two independent, though temporally coupled, motor programs (Jeannerod 1984). In the first experiment of the present study, subjects were required to reach out and grasp objects, with or without on-line, visual feedback. Object size and distance were covaried in a within-subjects design, and it was found that both grip formation and reach kinematics were affected by the manipulation of either variable. These data suggest that the control mechanisms underlying transport of the limb and grip formation are affected by similar task constraints. It was also observed that when visual feedback was unavailable after movement onset subjects showed an exaggerated opening of their hands, although grip size continued to be scaled for object size. The question remained as to whether the larger opening of the hand during no-feedback trials reflected the lack of opportunity to fine-tune the opening of the hand on-line, or the adoption of a strategy designed to increase tolerance for initial programming errors. To address this question, a second experiment was carried out in which we manipulated the predictability of visual feedback by presenting feedback and no-feedback trials in a random order. In contrast to the situation in which feedback and no-feedback trials were presented in separate blocks of trials (Exp. 1), in the randomly ordered series of trials presented in Exp. 2, subjects always behaved as if they were reaching without vision, even on trials where visual feedback was continuously available. These findings suggest that subjects adopt different strategies on the basis of the predictability of visual feedback, although there is nothing to suggest that this takes place at a conscious, or voluntary, level. The results of both experiments are consistent with the notion of a hierarchically-organized motor control center, responsible for optimizing performance under a variety of conditions through the coordination of different effector systems and the anticipation of operating constraints.

Separate neural pathways for the visual analysis of object shape in perception and prehension

BACKGROUND Earlier work with neurological patients has shown that the visual perception of object size and orientation depends on visual pathways in the cerebral cortex that are separate from those mediating the use of these same object properties in the control of goal-directed grasping. We present evidence suggesting that the same dissociation between perception and action is evident in the visual processing of object shape. In other words, discrimination between objects on the basis of their shape appears to be mediated by visual mechanisms that are functionally and neurally distinct from those controlling the pre-shaping of the hand during grasping movements directed at those same objects. RESULTS We studied two patients with lesions in different parts of the cerebral visual pathways. One patient (RV), who had sustained bilateral lesions of the occipitoparietal cortex, was unable to use visual information to place her fingers correctly on the circumference of irregularly shaped objects when asked to pick them up, even though she had no difficulty in visually discriminating one such object from another. Conversely, a second patient (DF), who had bilateral damage in the ventrolateral occipital region, had no difficulty in placing her fingers on appropriate opposition points during grasping, even though she was unable to discriminate visually amongst such objects. CONCLUSIONS This double dissociation lends strong support to the idea that the visual mechanisms mediating the perception of objects are functionally and neurally distinct from those mediating the control of skilled actions directed at those objects. It also supports the recent proposal of Goodale and Milner that visual perception depends on a ventral stream of projections from the primary visual cortex to the inferotemporal cortex, whereas the visual control of skilled actions depends on a dorsal stream from the primary visual cortex to the posterior parietal cortex.

Chapter 28 Visual pathways to perception and action

Publisher Summary There appears to be important integrative areas within the superior temporal sulcus in the monkey where a great deal of the necessary interaction to ensure behavioral and perceptual unity. Indeed there are many polysensory neurons in these areas, such that not only visual but also cross-modal perceptual integration may be enabled by these networks. Despite the crosstalk between the dorsal and ventral streams, the chapter discusses that each stream uses visual information in different ways. Both streams process information about orientation and shape, and probably about spatial relationships, including depth; and both are subject to the modulatory influences of an animals shifting spatial attention. The ventral stream provide object-centered coding, while the dorsal provide entirely viewer-centered information: the former would enable a monkey to identify an object as being of an edible type, the latter to guide its actions in picking it up. Although there will be differences in the ways that visual information is processed in the two systems, these differences are not a reflection of some biologically arbitrary separation of inputs, but rather a consequence of the special transformations required for perception and action, respectively.

An evolving view of duplex vision: separate but interacting cortical pathways for perception and action

In 1992, Goodale and Milner proposed a division of labour in the visual pathways of the primate cerebral cortex between a dorsal stream specialised for the visual control of action and a ventral stream dedicated to the perception of the visual world. In the years since this original proposal, support for the perception-action hypothesis has come from neuroimaging experiments, human neuropsychology, monkey neurophysiology, and human psychophysical experiments. Indeed, some of the strongest support for this hypothesis has come from behavioural experiments showing that visually guided actions are largely refractory to perceptual illusions. Although controversial, the findings from this literature both support the original hypothesis and suggest important modifications. The ongoing challenge for neurobiologists is to map these behavioural findings onto their corresponding neural substrates.

FMRI evidence for a 'parietal reach region' in the human brain

Event-related functional magnetic resonance imaging was used to examine activation in the posterior parietal cortex when subjects made pointing movements or saccades to the same spatial location. One region, well positioned to be homologous to the monkey parietal reach region (PRR), responded preferentially during memory-delay trials in which the subject planned to point to a specific location as compared to trials in which the subject planned to make a saccade to that same location. We therefore conclude that activation in this region is related to specific motor intent; i.e. it encodes information related to the subjects intention to make a specific movement to a particular spatial location.

Human fMRI evidence for the neural correlates of preparatory set

We used functional magnetic resonance imaging (fMRI) to study readiness and intention signals in frontal and parietal areas that have been implicated in planning saccadic eye movements—the frontal eye fields (FEF) and intraparietal sulcus (IPS). To track fMRI signal changes correlated with readiness to act, we used an event-related design with variable gap periods between disappearance of the fixation point and appearance of the target. To track changes associated with intention, subjects were instructed before the gap period to make either a pro-saccade (look at target) or an anti-saccade (look away from target). FEF activation increased during the gap period and was higher for anti- than for pro-saccade trials. No signal increases were observed during the gap period in the IPS. Our findings suggest that within the frontoparietal networks that control saccade generation, the human FEF, but not the IPS, is critically involved in preparatory set, coding both the readiness and intention to perform a particular movement.

A kinematic analysis of reaching and grasping movements in a patient recovering from optic ataxia

A detailed, kinematic analysis revealed subtle deficits in midline pointing and prehension in a patient showing good clinical signs of recovery from optic ataxia associated with bilateral parietooccipital damage. Relative to control subjects, the patient tended to misreach to the left with her right hand, and to the right with her left hand on a pointing task. While reach kinematics were otherwise normal in the pointing task, they were markedly disturbed in a prehension task, in which reaching and grasping movements must be integrated. In addition, difficulties in making fine postural adjustments to the hands were still evident 17 months post-injury. These findings suggest an important role for the posterior parietal lobes in programming goal-directed manual movements, and have implications for current theories of motor control and visual perception.