The effect of bilateral isometric forces in different directions on motor cortical function in humans

Abstract

The activity in the primary motor cortex (M1) reflects the direction of movements, but little is known about physiological changes in the M1 during generation of bilateral isometric forces in different directions. Here, we used transcranial magnetic stimulation to examine motor evoked potentials (MEPs), short-interval intracortical inhibition (SICI), and interhemispheric inhibition (IHI) in the left first dorsal interosseous (FDI) during isometric index finger abduction while the right index finger remained at rest or performed isometric forces in different directions (abduction or adduction) and in different postures (prone and supine). Left FDI MEPs were suppressed during bilateral compared with unilateral forces, with a stronger suppression when the right index finger force was exerted in the adduction direction regardless of hand posture. IHI targeting the left FDI increased during bilateral compared with unilateral forces and this increase was stronger during right index finger adduction despite the posture of the right hand. SICI decreased to a similar extent during both bilateral forces in both hand postures. Thus generation of index finger isometric forces away from the body midline (adduction direction), regardless of the muscle engaged in the task, down-regulates corticospinal output in the contralateral active hand to a greater extent than forces exerted toward the body midline (abduction direction). Transcallosal inhibition, but not GABAergic intracortical circuits, was modulated by the direction of the force. These findings suggest that during generation of bimanual isometric forces the M1 is driven by "extrinsic" parameters related to the hand action.

Fig. 1.

Experimental setup. A: diagram showing the visual display presented to all subjects during testing of unilateral and bilateral isometric index finger forces. Subjects were instructed on a monitor to perform 10% of left maximal isometric index finger abduction (10% ABD), whereas the right index finger remained at rest (0% Rest) or performed 30% of maximal isometric index finger abduction (30% ABD) or adduction (30% ADD) while motor evoked potentials (MEPs), interhemipheric inhibition (IHI), and short-interval intracortical inhibition (SICI) were tested in the left index finger. The condition in which the right hand remained at rest was used as baseline. The black vertical bar is the cursor that subjects were instructed to move by performing left and right isometric forces. The “GO” signal (gray box located to the left or to the right of the cursor) was the target to which subjects had to move the cursor. The distance between cursor and target is related to the magnitude of force required to accomplish each task, normalized to the maximal voluntary effort determined in each participant. B: schematic of the experimental setup showing the posture of both hands during testing. The left hand was always positioned in prone posture (palm down), whereas the right hand was positioned in prone or supine (palm up) posture. Then, when the right index finger performed ABD in the prone position the first dorsal interosseous (FDI) muscle was acting as an agonist to the task, whereas when the right index finger performed ABD in the supine position the FDI muscle was acting as an antagonist to the task.

Fig. 2.

Motor evoked potentials (MEPs). A: MEPs recorded from the left FDI of a representative subject during 10% of left ABD, whereas the right index finger remained at rest (baseline) or performed 30% of ABD or ADD. The specific action completed by the right index finger is indicated as Baseline, ABD, and ADD. In this example the right hand was positioned in prone posture. B: group data (n = 12). The abscissa shows the action completed by the right index finger in prone (black bars) and supine (white bars) postures. The ordinate shows left FDI MEP amplitudes as a percentage of the baseline left FDI MEPs measured with the right index finger at rest. The horizontal dashed line represents the left FDI MEP baseline measure with the right index finger at rest. Note the larger attenuation of the left FDI MEPs during both right hand postures during right ADD compared with right ABD contractions. Error bars indicate SEs. *P < 0.05. Note the left FDI MEP amplitudes were suppressed with respect to the baseline in all conditions (¥ indicates significant difference with respect to baseline).

Fig. 3.

Interhemispheric inhibition (IHI). A: IHI recorded from the left FDI of a representative subject during 10% of left ABD, whereas the right index finger remained at rest (baseline) or performed 30% of ABD or ADD. The actions by the right index finger are indicated as Baseline, ABD, and ADD. In this example the right hand was positioned in prone posture. Test MEP and conditioned MEP (Cond. MEP) are indicated by arrows. B: group data (n = 12). The abscissa shows the conditions tested during the assessment of IHI contractions in prone (black bars) and supine (white bars) postures. The ordinate indicates the magnitude of the conditioned MEP expressed as a percentage of the Test MEP [(Conditioned MEP × 100)/(Test MEP)] during bilateral isometric forces. The horizontal dashed line represents the size of the Test MEP. Note that IHI was increased to a larger extent during ADD forces regardless of the right hand posture. Error bars indicate SEs. *P < 0.05. Also note that IHI was significantly increased with respect to the baseline in all conditions tested (¥ indicates significant difference with respect to baseline).

Fig. 4.

Short-interval intracortical inhibition (SICI). A: SICI recorded from the left FDI of a representative subject during 10% of left ABD, whereas the right index finger remained at rest (baseline) or performed 30% of ABD or ADD. The actions by the right index finger are indicated as Baseline, ABD, and ADD. In this example the right hand was positioned in prone posture. Test MEP and conditioned MEP (Cond. MEP) are indicated by arrows. B: group data (n = 12). The abscissa shows all conditions tested during the assessment of SICI in prone (black bars) and supine (white bars) postures. The ordinate indicates the magnitude of the conditioned MEP expressed as a percentage of the Test MEP [(Conditioned MEP × 100)/(Test MEP)] during bilateral activation. The horizontal dashed line represents the size of the Test MEP. Note that the magnitude of SICI was decreased to a similar extent during both bilateral forces in both right hand postures. Error bars indicate SEs. *P < 0.05. Also note that SICI was significantly decreased with respect to the baseline in all conditions tested (¥ indicates significant difference with respect to baseline).

Fig. 5.

Relationship between IHI and SICI measurements. Graphs A and C show the magnitude of the Test MEP during bilateral isometric forces during assessment of IHI and SICI, respectively. We indicate the actions by the right index finger as ABD (abscissa) and ADD (ordinate). Note that subjects who had larger left FDI Test MEPs during right ABD also had larger Test MEPs during right ADD during IHI and SICI measurements. Graphs B and D show the magnitude of IHI and SICI [(Conditioned MEP × 100)/(Test MEP)], respectively, during bilateral isometric forces. The action completed by the right index finger is indicated as ABD (abscissa) and ADD (ordinate). Note that changes in SICI during both bilateral forces were not associated with the other measurements.