Muscles in "concert": study of primary motor cortex upper limb functional topography

Abstract

Background: Previous studies with Transcranial Magnetic Stimulation (TMS) have focused on the cortical representation of limited group of muscles. No attempts have been carried out so far to get simultaneous recordings from hand, forearm and arm with TMS in order to disentangle a 'functional' map providing information on the rules orchestrating muscle coupling and overlap. The aim of the present study is to disentangle functional associations between 12 upper limb muscles using two measures: cortical overlapping and cortical covariation of each pair of muscles. Interhemispheric differences and the influence of posture were evaluated as well.

Methodology/principal findings: TMS mapping studies of 12 muscles belonging to hand, forearm and arm were performed. Findings demonstrate significant differences between the 66 pairs of muscles in terms of cortical overlapping: extremely high for hand-forearm muscles and very low for arm vs hand/forearm muscles. When right and left hemispheres were compared, overlapping between all possible pairs of muscles in the left hemisphere (62.5%) was significantly higher than in the right one (53.5% ). The arm/hand posture influenced both measures of cortical association, the effect of Position being significant [p = .021] on overlapping, resulting in 59.5% with prone vs 53.2% with supine hand, but only for pairs of muscles belonging to hand and forearm, while no changes occurred in the overlapping of proximal muscles with those of more distal districts.

Conclusions/significance: Larger overlapping in the left hemisphere could be related to its lifetime higher training of all twelve muscles studied with respect to the right hemisphere, resulting in larger intra-cortical connectivity within primary motor cortex. Altogether, findings with prone hand might be ascribed to mechanisms facilitating coupling of muscles for object grasping and lifting -with more proximal involvement for joint stabilization- compared to supine hand facilitating actions like catching. TMS multiple-muscle mapping studies permit a better understanding of motor control and 'plastic' reorganization of motor system.

Figure 1. Experimental setting and electrode positioning for simultaneous MEP recordings from the examined muscles.

Figure 2. Original MEPs obtained from 12 muscles simultaneously at a two different stimulation sites, corresponding to: left panel, hot-spot of FDI (with respect to Cz, x = 3 cm, y = 2 cm); right panel, hot-spot of Deltoid (with respect to Cz, x = 1 cm, y = 2 cm); time and amplitude calibrations are 20 msec and 200 microV respectively.

Figure 3. TMS-MRI integration: number of co-activated muscles for each scalp position in a paradigmatic subject.

Figure 4. Covariation measure of each pair between the 12 examined muscles.

This measure was obtained from the right hemisphere of 10 healthy subjects lying with prone hands.

Figure 5. Inter-hemispheric comparison of co-activation and covariation measures (obtained with hand in prone position) between pairs of muscles belonging to three different districts (hand, forearm, arm).

Figure 6. Inter-position comparison of co-activation and covariation measures (obtained from the right hemisphere) between pairs of muscles belonging to three different districts (hand, forearm, arm).