Is that near my hand? Multisensory representation of peripersonal space in human intraparietal sulcus

Abstract

Our ability to interact with the immediate surroundings depends not only on an adequate representation of external space but also on our ability to represent the location of objects with respect to our own body and especially to our hands. Indeed, electrophysiological studies in monkeys revealed multimodal neurons with spatially corresponding tactile and visual receptive fields in a number of brain areas, suggesting a representation of visual peripersonal space with respect to the body. In this functional magnetic resonance imaging study, we localized areas in human intraparietal sulcus (IPS) and lateral occipital complex (LOC) that represent nearby visual space with respect to the hands (perihand space), by contrasting the response to a ball moving near-to versus far-from the hands. Furthermore, by independently manipulating sensory information about the hand, in the visual (using a dummy hand) and proprioceptive domains (by changing the unseen hand position), we determined the sensory contributions to the representation of hand-centered space. In the posterior IPS, the visual contribution was dominant, overriding proprioceptive information. Surprisingly, regions within LOC also displayed visually dominant, hand-related activation. In contrast, the anterior IPS was characterized by a proprioceptive representation of the hand, as well as showing tactile hand-specific activation, suggesting a homology with monkey parietal hand-centered areas. We therefore suggest that, whereas cortical regions within the posterior IPS and LOC represent hand-centered space in a predominantly visual manner, the anterior IPS uses multisensory information in representing perihand space.

Figure 1.

Experimental setup: a 2 × 2 × 2 factorial design. A schematic illustration of the experimental conditions is shown. In each experiment, a moving ball was presented in either of two positions, near or far (with respect to the hand), while the subject was maintaining fixation between the two targets. Proprioceptive and visual information about hand position with respect to the near condition were manipulated between experiments. A, Real-hand experiment: having congruent visual and proprioceptive information. B, Occluded-hand experiment: proprioceptive information only. C, Dummy-hand experiment: illusory visual information. D, Retracted-hand experiment: with the hand away from the near target.

Figure 2.

ROI analysis: model predictions. A schematic illustration of the expected hemodynamic relationship between the near (light lines) and far (dark lines) conditions across four different experiments. A, When the preference for the near condition is consistent regardless of visual and proprioceptive hand position information. B, When the preference for the near condition is observed only when visual information of the hand (real or dummy) indicates its position close to the near target. C, If the preference for the near condition is present only when there is proprioceptive information that the hand is positioned close to the near target.

Figure 3.

Group results: determining the relative contributions of visual and proprioceptive information to the hand schema. fMRI differential activation (whole brain corrected, p < 0.05) for near versus far stimuli on representative inflated and unfolded maps of the right hemisphere (RH) and left hemisphere (LH). Shown are the areas with preference for the ball approaching the near target. A, When next to the subject's hand. B, When the subject's hand was occluded from sight. C, When a dummy hand was placed at the same position as the occluded hand, while the subject's own hand was retracted. D, When the subject's hand was retracted away from the near target. The comparison between the activation preference in the different experiments enables identification of putative hand-related areas in the cortex, as well as the factors (visual or proprioceptive) governing the hand position-related representation. Note that the mere presence of the dummy hand modulated parietal areas in a similar way to the real hand. A, Anterior; P, posterior; CS, central sulcus; ColS, collateral sulcus.

Figure 4.

Tactile properties of the hand-related visual areas. Activation on an inflated whole-brain map (shown in orange) represents areas that significantly responded to a tactile stimulus on the subject's left hand. We present only voxels that also show a preference for the near ball over the far in the real-hand experiment (in the absence of any tactile input; green lines). Areas showing preference for the near ball with illusory visual information of the hand position (dummy-hand experiment) are shown in pink. Note that there is little overlap between the tactile areas and the areas modulated by the seen (dummy or real) hand position. LH, Left hemisphere; RH, right hemisphere; CS, central sulcus. Cluster corrected (p < 0.05).

Figure 5.

ROI analysis: posterior IPS. A, Areas showing significant preference for the near over the far condition in the real-hand experiment superimposed on a representative inflated right hemisphere. The white-filled circle represents the average location (center of gravity) of the ROI between subjects. B, Averaged hemodynamic response curves of the percentage signal change for the near condition (dark colors) and the far condition (light colors). For each subject, clusters of voxels showing significantly greater activation for the near (compared with the far) condition in the real-hand experiment (within the posterior IPS) were selected as the ROI. These clusters were then closely examined in the three other experiments. The gray background denotes the time of presentation of the visual stimuli (in seconds). Asterisks denote statistical significance between the averaged time courses: *p < 0.05; **p < 0.01. Note that the visual presence of the (dummy or real) hand modulates the response of the region to the visual stimuli.

Figure 6.

ROI analysis: anterior IPS. Notations are as in Figure 5. Note that the proprioceptive information of hand position (next to the near target) modulates the response of the region to the visual stimuli.

Figure 7.

ROI analysis: LOC. Notations are as in Figure 5.

Figure 8.

Attentional control: placing the dummy hand outside perihand space. Areas showing preference for the near over the far ball (reds) and for the far ball (blues) over the near ball in the far-dummy-hand experiment (solid patches) and in the retracted-hand experiment (outline patches) are shown. Note that the two experiments differ only in the presence of the dummy hand by the far target. The overlap in responses in the two experiments suggests that, when the dummy hand is placed out of peripersonal space, it does not affect hand-related areas, as would be expected if the modulation was attributable to attention referred to the dummy hand. CS, Central sulcus.