Virtual lesion of angular gyrus disrupts the relationship between visuoproprioceptive weighting and realignment

Abstract

Posterior parietal cortex is thought to be involved in multisensory processes such as sensory weighting (how much different modalities are represented in sensory integration) and realignment (recalibrating the estimates given by unisensory inputs relative to each other, e.g., when viewing the hand through prisms). Sensory weighting and realignment are biologically independent but can be correlated such that the lowest-weighted modality realigns most. This is important for movement precision because it results in the brain's estimate of hand position favoring the more reliable (higher-weighted) modality. It is unknown if this interaction is an emergent property of separate neural pathways for weighting and realignment or if it is actively mediated by a common substrate. We applied disruptive TMS to the angular gyrus near the intraparietal sulcus (PGa) before participants performed a task with misaligned visual and proprioceptive information about hand position. Visuoproprioceptive weighting and realignment were unaffected. However, the relationship between weighting and realignment, found in control conditions, was absent after TMS in the angular gyrus location. This suggests that a specific region in the angular gyrus actively mediates the interaction between visuoproprioceptive weighting and realignment and may thus play a role in the decreased movement precision associated with posterior parietal lesions.

Figure 1

(A) Potential substrates of the visuoproprioceptive weighting and realignment correlation. The first possibility (1) is that the two processes occur independently (Block & Bastian, 2011) and a correlation is found because the same environmental signals contribute to both computations. Under this hypothesis, disruption of angular gyrus by cTBS should have no effect on the weighting–realignment correlation unless this area is important for weighting (dashed green line), realignment (dotted green line), or both (solid green line). A second possibility (2) is that the correlation of weighting and realignment is actively mediated by a separate neural substrate. This hypothesis predicts that if that substrate includes the angular gyrus location studied here, then cTBS in the AG group should disrupt the weighting–realignment correlation (without specifically affecting weighting or realignment). (B) Sample of cTBS stimulation location in an AG participant. 3-D reconstruction of the surface of the participant’s brain, with the locations of cTBS in all three groups indicated by arrows. In the AG group, cTBS location (Talairach coordinates [50 −50 40]; Clower et al. 1996) fell on the angular gyrus (PGa), close to the border between BA 39 and BA 40 (white circle). Pz and Sham cTBS were applied at Pz and Cz based on the 10–20 EEG system, respectively.

Figure 2

Experimental setup and time course. (A) Timeline of the experiment. TMS1: We determined RMT and SI1 mV response. Base 1: Baseline block of reaching with no visuoproprioceptive misalignment. TMS2 (cTBS): The participant received cTBS. Base 2: A second baseline block (no visuoproprioceptive misalignment) to evaluate any changes in reaching behavior that resulted from cTBS. Adaptation: Reaching with a gradually imposed visuoproprioceptive misalignment. TMS3: We determined RMT and 1 mV response a second time to evaluate whether any changes in corticospinal excitability occurred. Blue lines represent position of V targets (and V component of VP targets) in the y dimension (in mm). Red dashed lines represent position of P targets (and P component of VP targets) in the y dimension (in mm). (B) Participants looked into a horizontal mirror (middle) and saw targets and cursors indicating hand position reflected from a horizontal rear projection screen (top). The reaching hand rested on a surface (bottom) below the mirror. The (nondominant) target hand remained below the reaching surface at all times. The mirror was positioned midway between screen and reaching surface, such that images in the mirror appeared to be in the plane of the reaching surface. (C) Bird’s eye view of the display before reaches to VP, P, and V targets early (Row 1) and late (Row 2) in the Adaptation block. Participants first placed their reaching finger (white dashed line) in the yellow start box with the aid of a blue cursor indicating reaching finger position (veridical to minimize proprioceptive drift between reaches; Wann & Ibrahim, 1992). Participants positioned their target finger (dashed gray line) as instructed: On one of two tactile markers stuck to the bottom of the reaching surface about 40 mm apart (green dashed circles) for a VP (column 1) or P (column 2) target or down in their lap for a V target (column 3), which appeared as a white square. For VP reaches, the V target was projected on the P target during the baseline blocks but was gradually offset in the y direction during the adaptation block (Row 2). Only the yellow start position, white V target, and blue cursor were visible to the participant, and the cursor disappeared at reach initiation. Movement speed was not restricted, and participants were permitted to make adjustments.

Figure 3

Individual and group results showed no significant effect on visual or proprioceptive realignment. (A–C) Samples of representative participants for each group. Reach endpoints in XY to visual (blue), proprioceptive (red), and combined (purple) targets (targets at the origin). Ellipses reflect 90% confidence intervals. Although we calculated weight of vision versus proprioception (w_v) on a trial-by-trial basis, it is possible to see from the confidence ellipses that for the AG participant in (A), the VP endpoints better match the V endpoints, reflecting a high w_v. Conversely, for the two Sham (B) and Pz (C) participants, VP endpoints better match the P endpoints, reflecting a lower w_v. (D–F) Reach endpoints in the y dimension to visual (blue), proprioceptive (red), and combined (purple) targets in the Adaptation block. Dashed gray line indicates that P targets did not shift during adaptation, but V targets (solid gray line) did, to a maximum of 70 mm away from P targets by the end of Adaptation. A shift in P endpoints (dashed red line) from P targets signifies proprioceptive realignment (Δŷ_P). If V endpoints (blue line) fall short of V targets (solid gray line), visual realignment (Δŷ_V) is implied. (A) This AG participant realigned proprioception (red line, Δŷ_P = 8.ŷ mm) and vision (blue line, Δŷ_V = ŷ9.6 mm). (B) This Sham participant realigned proprioception 6.7 mm and vision ŷ6.5 mm. (C) This Pz participant realigned proprioception 8.4 mm and vision 32.5 mm. (G–I) Group mean reach endpoints, with standard error (shaded regions). Insets: magnitude of group mean proprioceptive (red) and visual (blue) realignment, with standard error. There were no significant differences across groups over time, suggesting that cTBS did not affect V or P realignment differently in different groups.

Figure 4

Relationship between weighting and realignment was disrupted in AG group. Proprioceptive realignment (Δŷ_P) and weight of vision (w_v) are significantly correlated during Adaptation in Sham (B) and Pz (C) groups, but not in the AG group (A). This indicates that cTBS in the AG group disrupted the relationship between visuoproprioceptive weight and realignment. Dashed line represents the best fit line for a similar experiment in Block and Bastian (2011); with 19 participants, the correlation r was .55 (p = .01). Open circles represent the sample participants in Figure 3A–F.