Human parietal cortex in action

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Experiments using functional neuroimaging and transcranial magnetic stimulation in humans have revealed regions of the parietal lobes that are specialized for particular visuomotor actions, such as reaching, grasping and eye movements. In addition, the human parietal cortex is recruited by processing and perception of action-related information, even when no overt action occurs. Such information can include object shape and orientation, knowledge about how tools are employed and the understanding of actions made by other individuals. We review the known subregions of the human posterior parietal cortex and the principles behind their organization.

Introduction

Sensory control of actions depends crucially on the posterior parietal cortex, that is, all of the parietal cortex behind primary (SI) and secondary (SII) somatosensory cortex, including both the superior and inferior parietal lobules, which are divided by the intraparietal sulcus. Initially posterior parietal cortex was considered part of ‘association cortex’, which integrates information from multiple senses. During the past decade, the role of the posterior parietal cortex in space perception and guiding actions was emphasized [1, 2]. Electrophysiological studies in the macaque monkey defined a mosaic of small areas, each specialized for a particular type of action of the eyes, head, arm or hand [3]. Because neuroimaging in humans has enabled more precise localization of functional areas, it is increasingly apparent that the human parietal cortex contains a similar mosaic of specialized areas. Several years ago we reviewed the early evidence for possible functional equivalencies between macaque and human regions of the posterior parietal cortex, particularly within the intraparietal sulcus [4], however, since then the relationships have become considerably clearer. This owes, in large part, to the rapid growth of neuroimaging studies, particularly experiments using functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS).

In one popular view of the visual system [1], visual information is segregated along two pathways: the ventral stream (occipito-temporal cortex) computes vision for perception, whereas the dorsal stream (occipito-parietal cortex) computes vision for action. Here, we review recent advances that address the organization of the posterior parietal cortex and the action-related subregions within it. We begin by focusing on the role of the dorsal stream in visually-guided real actions. However, we then discuss a topic that does not fit so easily into the dichotomy: action-related perceptual tasks that invoke the dorsal stream. Growing evidence from studies in both macaque and human brains suggests that areas within the posterior parietal cortex might be active not only when the individual is preparing to act, but also during observation of others’ actions and the perceptual processing of attributes and affordances that are relevant to the actions, even when no actions are executed. We focus largely on the human brain, but include a brief summary of comparable areas in the macaque monkey brain and potential homologies between the two species (See Figure 1). The latest advances in the study of the macaque posterior parietal cortex [3] and issues of macaque–human homology [5, 6, 7] were recently highlighted elsewhere.

Section snippets

Reaching and pointing

The role of the posterior parietal cortex in reaching is evident from the deficits in patients with optic ataxia [8]. Typically these patients show inaccurate reaches only when visual targets are viewed in peripheral vision. The lesions underlying optic ataxia were classically assigned to the parietal lobe, always including the intraparietal sulcus and sometimes extending into the inferior or superior parietal lobules [9]. Karnath and Perenin [10] were recently able to identify more specific

Object-selective areas

Although the vast majority of human studies on object selectivity focused on areas within the ventral stream [47], neuroimaging has also revealed shape-selective activation for objects within the dorsal stream of both monkeys and humans [48]. These regions tend to be ignored because of concerns regarding attentional confounds, which could be more problematic for parietal areas than for occipito-temporal areas. Given the importance of actions in the dorsal stream, we hypothesize that these

Conclusions

Mapping of the human dorsal stream has progressed at a slower pace than mapping of the ventral stream, largely because of the technical challenges of using action paradigms for neuroimaging, perhaps accompanied by a general neglect of the study of actions in cognitive science [80]. In some ways, however, this might be an advantage, because the study of the ventral stream has revealed general principles that might also be helpful in elucidating organization within the dorsal stream.

Within both

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was funded by operating grants to JC Culham from the Natural Sciences and Engineering Research Council of Canada and the Canadian Institutes of Health Research. We thank C Cavina-Pratesi, P Medendorp, M-T Perenin, G Króliczak, and the editors of this volume for comments on an earlier draft of the manuscript. We would also like to thank S Everling for providing the anatomical data from a macaque monkey brain which was used for the cortical reconstruction in the figure.

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