Synchrony of hand-foot coupled movements: is it attained by mutual feedback entrainment or by independent linkage of each limb to a common rhythm generator?

Abstract

BACKGROUND: Synchrony of coupled oscillations of ipsilateral hand and foot may be achieved by controlling the interlimb phase difference through a crossed kinaesthetic feedback between the two limbs, or by an independent linkage of each limb cycle to a common clock signal. These alternative models may be experimentally challenged by comparing the behaviour of the two limbs when they oscillate following an external time giver, either alone or coupled together. RESULTS: Ten subjects oscillated their right hand and foot both alone and coupled (iso- or antidirectionally), paced by a metronome. Wrist and ankle angular position and Electromyograms (EMG) from the respective flexor and extensor muscles were recorded. Three phase delays were measured: i) the clk-mov delay, between the clock (metronome beat) and the oscillation peak; ii) the neur (neural) delay, between the clock and the motoneurone excitatory input, as inferred from the EMG onset; and iii) the mech (mechanical) delay between the EMG onset and the corresponding point of the limb oscillation. During uncoupled oscillations (0.4 Hz to 3.0 Hz), the mech delay increased from -7° to -111° (hand) and from -4° to -83° (foot). In contrast, the clk-mov delay remained constant and close to zero in either limb since a progressive advance of the motoneurone activation on the pacing beat (neur advance) compensated for the increasing mech delay. Adding an inertial load to either extremity induced a frequency dependent increase of the limb mechanical delay that could not be completely compensated by the increase of the neural phase advance, resulting in a frequency dependent increment of clk-mov delay of the hampered limb. When limb oscillations were iso- or antidirectionally coupled, either in the loaded or unloaded condition, the three delays did not significantly change with respect to values measured when limbs were moved separately. CONCLUSION: The absence of any significant effect of limb coupling on the measured delays suggests that during hand-foot oscillations, both iso- and antidirectionally coupled, each limb is synchronised to the common rhythm generator by a "private" position control, with no need for a crossed feedback interaction between limbs