Impairment in the control of coupled cyclic movements of ipsilateral hand and foot after total callosotomy

Abstract

Integrity of both cerebral hemispheres is required to control in-phase or anti-phase coupling of ipsilateral hand and foot oscillations, as shown by the impairment of these tasks when performed on the healthy side of hemiplegic patients. On this basis, coupling of hand–foot movements was analysed in a right-handed subject (ME) who underwent a total resection of the corpus callosum. Oscillations of the prone hand and foot, paced by a metronome at different frequencies, as well as EMG activity in extensor carpi radialis (ECR) and tibialis anterior (TA) muscles were analysed by measuring the average phase difference between the hand and foot movements and EMG cycles. ME performed in-phase movements (right-hand extension coupled to right-foot dorsal flexion) at frequencies up to 3 Hz, though the hand cycle progressively lagged the foot cycle as the frequency increased. At 3 Hz the hand lag reached −142° (as compared to about 25° in healthy subjects). The lag increased even further after application of an inertial load to the hand, reaching 180° at 1.8 Hz (about 50° in healthy subjects). ME's hand lag is caused by the lack of any anticipatory reaction in hand movers. In contrast to healthy subjects, which activate the ECR earlier than the TA when the frequency increases, ME activated the ECR later than TA at all frequencies higher than 0.9 Hz. Anti-phase movements (hand extension coupled to foot plantar flexion) were performed only upto 1 Hz in unloaded conditions. At 0.6 Hz, movements were in tight phase-opposition (3°), but at 1 Hz, the hand lag reached −34° because of a delayed ECR activation. After hand loading ME was unable to couple movements in anti-phase. In contrast, normal subjects maintain a tight anti-phase coupling up to 2.0 Hz, both with an unloaded or loaded hand. Similar deficits were observed by ME when performing in-phase and anti-phase coupling on the left side, as well as when he was blindfolded. In normal subjects, an anticipated muscular activation of hand movers compensates for hand loading. Since this compensation must depend on monitoring the hand delay induced by loading, the absence in ME of such compensatory reaction suggests that callosal division had apparently compromised the mechanisms sustaining feedback compensation for differences in the biomechanical limb properties. They also confirm and reinforce the idea that elaboration of the afferent message, aiming at controlling the phase of the movement association, needs the co-operation of both cerebral hemispheres.