Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp - PubMed (original) (raw)
Comparative Study
Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp
Eugene Tunik et al. Nat Neurosci. 2005 Apr.
Abstract
Adaptive motor behavior requires efficient error detection and correction. The posterior parietal cortex is critical for on-line control of reach-to-grasp movements. Here we show a causal relationship between disruption of cortical activity within the anterior intraparietal sulcus (aIPS) by transcranial magnetic stimulation (TMS) and disruption of goal-directed prehensile actions (either grip size or forearm rotation, depending on the task goal, with reaching preserved in either case). Deficits were elicited by applying TMS within 65 ms after object perturbation, which attributes a rapid control process on the basis of visual feedback to aIPS. No aperture deficits were produced when TMS was applied to a more caudal region within the intraparietal sulcus, to the parieto-occipital complex (putative V6, V6A) or to the hand area of primary motor cortex. We contend that aIPS is critical for dynamic error detection during goal-dependent reach-to-grasp action that is visually guided.
Conflict of interest statement
COMPETING INTERESTS STATEMENT
The authors declare that they have no competing financial interests.
Figures
Figure 1
Reach-to-grasp adjustments required in Experiments 1 and 2. In most trials, the object rotated 180° (unperturbed), leaving the grasp aperture or grasp orientation unperturbed (left column). In a minority of trials, the object rotated 90° (perturbed), necessitating either an increase in grasp aperture (Experiment 1) or a change in grasp orientation (Experiment 2). Also shown are placements of the infrared light–emitting diodes, which allow tracking of hand position.
Figure 2
Mean grasp aperture profiles for one subject in Experiment 1. Below each panel is the reconstructed three-dimensional image of the subject’s brain and the target site (white dot) over which the TMS coil was positioned. Profiles in the unperturbed and perturbed conditions are plotted as hatched and solid lines, respectively. Trials in which TMS was delivered early and late are plotted in blue and red, respectively. Vertical lines: T1 and T2, time of the early and late TMS pulse; M, time of the motor rotation. MC, primary motor cortex. POC, parieto-occipital complex. cIPS, caudal to aIPS near apex of IPS.
Figure 3
Mean aperture profiles for the remaining eight subjects (shown only for aIPS). Insets show the respective subject’s reconstructed three-dimensional brain image and the target site (white dot) over which the TMS coil was positioned. Profiles in the unperturbed and perturbed conditions are plotted as hatched and solid lines, respectively. Trials in which TMS was delivered early and late are plotted in blue and red, respectively. Vertical lines: T1 and T2, time of the early and late TMS pulse; M, time of the motor rotation.
Figure 4
Group mean (± s.e.m.) for grasp- and reach-related kinematics. (a–d) Shown is (a) the time to peak aperture, (b) the variance (s.d.) of the time to peak aperture, (c) the grasp movement time and (d) the reach movement time. Perturbed and unperturbed conditions are indicated by vertical and horizontal object orientations, respectively. The time of TMS delivery is indicated as either early or late. MC, primary motor cortex.
Figure 5
Mean (± s.d.) grasp movement times in Experiment 1a. Subjects S1, S3 and S8 received TMS to aIPS either 30, 65, 80 or 95 ms after the end of object rotation. Movement was significantly prolonged only when TMS was delivered at the 30 ms time point but not thereafter, suggesting that processing within aIPS may have been completed by 65 ms after object perturbation. Note the absence of this effect in the object–non-perturbed condition.
Figure 6
Movement kinematics for Experiment 2. (a) Mean profiles of the forearm (hand) rotation angle for eight subjects. The starting orientation is approximately 0°. The targeted orientation either remains 0° (in the unperturbed condition) or changes to about 90° (in the perturbed condition). Profiles in the unperturbed and perturbed conditions are plotted as hatched and solid lines, respectively. Trials in which TMS was delivered early and late are plotted in blue and red, respectively. Vertical lines: T1 and T2, time of the early and late TMS pulse; M, time of the motor rotation. (b) The mean time ± s.e.m. (n = 8) to rotate the forearm from the starting orientation (~0°) to match the final object orientation (~0° in the unperturbed case and ~90° in the perturbed case).
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References
- Johnson SH & Grafton ST From ‘acting on’ to ‘acting with’: the functional anatomy of object-oriented action schemata. Prog. Brain Res 142, 127–139 (2003). - PubMed
- Marconi B et al. Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb. Cortex 11, 513–527 (2001). - PubMed
- Rizzolatti G & Matelli M Two different streams form the dorsal visual system: anatomy and functions. Exp. Brain Res 153, 146–157 (2003). - PubMed
- Luppino G, Murata A, Govoni P & Matelli M Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4). Exp. Brain Res 128, 181–187 (1999). - PubMed
- Rizzolatti G & Luppino G The cortical motor system. Neuron 31, 889–901 (2001). - PubMed
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