Functional interplay between posterior parietal and ipsilateral motor cortex revealed by twin-coil transcranial magnetic stimulation during reach planning toward contralateral space

Abstract

Posterior parietal cortex (PPC) has connections with motor and premotor cortex, thought to transfer information relevant for planning movements in space. We used twin-coil transcranial magnetic stimulation (tcTMS) methods to show that the functional interplay between human right PPC and ipsilateral motor cortex (M1) varies with current motor plans. tcTMS during the reaction time of a reach task revealed facilitatory influences of right PPC on right M1 only when planning a (contralateral) leftward rather than rightward reach, at two specific time intervals (50 and 125 ms) after an auditory cue. The earlier reach-direction-specific facilitatory influence from PPC on M1 occurred when subjects were blindfolded or when the targets were presented briefly, so that visual feedback corrections could not occur. PPC-M1 interplay was similar within the left hemisphere but was specific to (contralateral) rightward planned reaches, with peaks at 50 and 100 ms. Functional interplay between human parietal and motor cortex is enhanced during early stages of planning a reach in the contralateral direction.

Figures

Figure 1.

A, Conditioning TMS stimulus was applied at 90% of RMT over PPC at a site corresponding to the AG near the cIPS. B, Facilitatory effects obtained at rest after PPC conditioning in subjects of experiment 1. The intensity of test stimulus was adjusted to evoke an MEP of ∼1 mV peak to peak in the relaxed left FDI. This M1 TMS could be preceded by a CS delivered 4 ms before over ipsilateral PPC at an intensity of 90% of RMT. Errors bars indicate SEM. *p < 0.05. C, Schematic representation of the reaching task. At trial onset, subjects fixated the central cross. After the imperative cue sound (onsetting randomly 1–3 s later), they reached to the left or right target with their left hand. TMS was delivered over M1 of the right hemisphere at different delays (25, 50, 75, 100, 125, and 150 ms) after the cue sound onset and thus before actual reach initiation. In half of the trials, M1 TMS was preceded 4 ms earlier by a PPC TMS pulse (intensity of 90% RMT).

Figure 2.

Effects of PPC conditioning on ipsilateral M1 excitability at different delays after the cue signal, when subjects planned left-hand reaches to visible targets on left or right. A, B, MEP amplitudes recorded from the left FDI during either conditions (single or paired-pulse TMS) at different time points after the imperative auditory cue, when leftward (A) or rightward (B) reaches were planned. Mean percentages of baseline MEP amplitude attributable to right PPC conditioning are shown in C, with 100% representing no change. Corticocortical PPC–M1facilitation occurred selectively at an early delay of 50 ms and at the later point of 125 ms after the auditory imperative cue for a leftward reach (yellow points in C). There was no facilitation when a rightward reach was planned (dark points in C). *p < 0.05, post hoc analysis. Errors bars indicate SEM.

Figure 3.

PPC–M1 functional connectivity during movement planning in space with subjects blindfolded (A) or when subjects were allowed to see briefly the targets before the acoustic cues (B). When subjects were not allowed to see peripheral targets (A), we found a similar profile of activation of PPC–M1 functional connectivity during the early phase of movement planning. Post hoc analysis showed that corticocortical facilitation using a conditioning intensity of 90% RMT with 4 ms interstimulus interval occurred selectively at an early delay of 50 ms after the auditory imperative signal, only for trials in which a contralateral left reach was reached. This pattern of activation of PPC–M1 connectivity was the same when subjects were allowed to see transiently the targets before they were asked to decide where to reach (B). Values are expressed as mean percentage for MEP amplitude attributable to right PPC conditioning. *p < 0.05, post hoc analysis. Errors bars indicate SEM.

Figure 4.

Comparison between results obtained in experiments 1 and 2 for the common delays, comparing the results obtained when subjects were planning a leftward movement with vision (Light) or when blindfolded (Dark). A late peak of facilitation at 125 ms for the PPC–M1hand interaction was evident only when subjects were able to see the peripheral targets. *p < 0.05, post hoc analysis. Errors bars indicate SEM. Note that significant facilitation (relative to the 100% baseline) was observed for both the light and the blindfolded condition at the early 50 ms delay.

Figure 5.

PPC–M1 functional connectivity is absent during saccade planning (experiment 3). PPC–M1 effects were not evident during a saccadic task. Unlike the reach tasks (experiments 1 and 2), there was now no significant facilitation at any time point. A, B, MEP amplitude recorded from the left FDI during either condition (single or paired-pulse TMS) at different time points when leftward (A) or rightward (B) saccades were planned. C, Normalized data (mean percentage values of MEP amplitude during right PPC conditioning, with 100% indicating no effect) obtained in experiments 1 and 3, comparing the results obtained when subjects were planning a leftward movement with either the hand or the eyes, respectively. The early peak of facilitation at 50 ms for the PPC–M1hand interaction was evident only when subjects were planning reaching movements toward the contralateral left side but not for planned saccades toward that side. *p < 0.05, post hoc analysis. Errors bars indicate SEM.

Figure 6.

Experiment 4: effects of left PPC conditioning on ipsilateral M1 excitability at different delays after the cue signal, when subjects planned right-hand reaches to visible targets on left or right. A, B, MEP amplitudes recorded from the right FDI during either conditions (single or paired-pulse TMS) at different time points after the imperative auditory cue, when leftward (A) or rightward (B) reaches were planned. Mean percentages of baseline MEP amplitude attributable to right PPC conditioning are shown in C, with 100% representing no change. Corticocortical PPC–M1 facilitation occurred selectively at an early delay of 50 and 100 ms after the auditory imperative cue for a contralateral rightward reach (dark points in C). There was no facilitation when a leftward reach was planned instead (light gray points in C). *p < 0.05, post hoc analysis. Errors bars indicate SEM.