Instabilities during antiphase bimanual movements: are ipsilateral pathways involved?

Abstract

The spatial and temporal coupling between the hands is known to be very robust during movements which use homologous muscles (in-phase or symmetric movements). In contrast, movements using nonhomologous muscles (antiphase or asymmetric movements) are less stable and exhibit a tendency to undergo a phase transition to in-phase movements as movement frequency increases. The instability during antiphase movements has been modeled in terms of signal interference mediated by the ipsilateral corticospinal pathways. In this study we report that participants in whom distal ipsilateral motor-evoked potentials could be elicited with transcranial magnetic stimulation (TMS), exhibited higher variability during a bimanual circling task than participants whose ipsilateral pathways could not be transcranially activated. These results suggest that ipsilateral control of the limb affects the level of bimanual coupling, and may contribute to uncoupling phenomena observed during asymmetric coordination.

Perception and action influences on discrete and reciprocal bimanual coordination

“…The tendency for participants to transition from asymmetric coordination patterns to in-phase movements of the fingers or limbs has been thought to be due, at least in part, to biases originating in the action component of the perception-action system (e.g., Kagerer et al, 2002Kagerer et al, , 2003Peper et al, 2008). For example, the concept of neural crosstalk has been used to explain the findings of stability differences and phase transitions in various bimanual coordination patterns based on interactions in the forward command streams in the highly interconnected and redundant organization of the nervous system (for review, see Swinnen, 2002).…”

“…According to the crosstalk model, two independent motor plans exist for each limb and some fraction of the force commands for one limb is diverted to the other limb (Cattaert et al, 1999). It has been proposed that the movements produced by the symmetric activation of homologous muscles are stabilized when the contralateral and ipsilateral signals are integrated, while movements produced by the activation of nonhomologous muscles or asymmetric activation suffer from ongoing interference due to conflicting information and partial intermingling of signals controlling the two arms (e.g., Kagerer et al, 2003;Kennedy, Boyle, Rhee, & Shea, 2015a;Marteniuk, MacKenzie, & Baba, 1984).…”

“…However, when an antiphase pattern is performed (requiring the simultaneous activation of non-homologous muscles), each limb (depending on the timing) will receive conflicting signals from the contralateral and ipsilateral hemisphere (Cattaert et al, 1999;Kagerer et al, 2003;Kennerley et al, 2002). Interestingly, the likelihood of interference resulting from non-congruent signals appears to increase as cycle frequency and/or force requirements increase and may even delay the onset of force commands (Kennedy, Wang, Shea, 2013a,b).…”

“…That is, relative phase patterns other than 0 o and 180 o are not inherently stable and the motor system shows a bias towards what has been labeled the intrinsic dynamics of in-phase and anti-phase coordination (Schöner & Kelso, 1988). A number of researchers have suggested that the tendency toward in-phase and anti-phase movements of the limbs originates in action constraints of the perception-action system (e.g., Kagerer, Summers, & Semjen, 2003;Kennerly, Diedrichsen, Hazeltine, Semjen, & Ivry, 2002;Peper, de Boer, de Poel, & Beek, 2008), while other researchers suggest that perceptual constraints can play a large role in determining the stability of the bimanual coordination pattern (e.g., Bingham, 2004a,b;Mechsner et al, 2001;Mechsner & Knoblich 2004). Alternately, a number of studies have favored the hypothesis that a coalition of constraints, ranging from high-level perceptual to lower-level motor, modulates the stability of coordinated behavior (e.g., Amazeen, DaSilva, & Amazeen, 2008;Carson & Kelso, 2004;Meesen, Wenderoth, Temprado, Summers, & Swinnen, 2006;Salesse, Temprado, & Swinnen, 2005;Temprado et al, 2003;Shea, Kovacs, & Buchanan, 2009;Swinnen, 2002;Swinnen & Wenderoth, 2004).…”

Movement Initiation-Locked Activity of the Anterior Putamen Predicts Future Movement Instability in Periodic Bimanual Movement

“…The difference in stability between the two modes can induce spontaneous phase transitions from the antiphase to the in-phase mode (Kelso, 1984) even when attempting to maintain an antiphase movement pattern, although the intentional component can stabilize an otherwise unstable antiphase pattern to some degree (Scholz and Kelso, 1990;Kelso, 1995;De Luca et al, 2010). In addition to the intentional component, the stability of antiphase movements also depends on learning (Temprado et al, 2002), perceptual bias (Mechsner et al, 2001), attention (Monno et al, 2000), and neural connections (Kennerley et al, 2002;Kagerer et al, 2003). Because the probability of these sudden errors differs between subjects (see Fig.…”