A coupled oscillator model of disordered interlimb coordination in patients with Parkinson's disease

Abstract

Coordination between the left and right limbs during cyclic movements, which can be characterized by the amplitude of each limb's oscillatory movement and relative phase, is impaired in patients with Parkinson's disease (PD). A pedaling exercise on an ergometer in a recent clinical study revealed several types of coordination disorder in PD patients. These include an irregular and burst-like amplitude modulation with intermittent changes in its relative phase, a typical sign of chaotic behavior in nonlinear dynamical systems. This clinical observation leads us to hypothesize that emergence of the rhythmic motor behaviors might be concerned with nonlinearity of an underlying dynamical system. In order to gain insight into this hypothesis, we consider a simple hard-wired central pattern generator model consisting of two identical oscillators connected by reciprocal inhibition. In the model, each oscillator acts as a neural half-center controlling movement of a single limb, either left or right, and receives a control input modeling a flow of descending signals from higher motor centers. When these two control inputs are tonic-constant and identical, the model has left-right symmetry and basically exhibits ordered coordination with an alternating periodic oscillation. We show that, depending on the intensities of these two control inputs and on the difference between them that introduces asymmetry into the model, the model can reproduce several behaviors observed in the clinical study. Bifurcation analysis of the model clarifies two possible mechanisms for the generation of disordered coordination in the model: one is the spontaneous symmetry-breaking bifurcation in the model with the left-right symmetry. The other is related to the degree of asymmetry reflecting the difference between the two control inputs. Finally, clinical implications by the model's dynamics are briefly discussed.

Unraveling Interlimb Interactions Underlying Bimanual Coordination

“…In addition, neurophysiological modeling studies have shown that salient stability-related phenomena in interlimb coordination (e.g., in-phase being more stable than antiphase; frequency-induced transitions between movement patterns) can arise in a system of two coupled neural oscillators in the absence of afferent feedback, yielding a dynamical account of integrated timing (Asai et al 2003;Grossberg et al 1997). However, afference-based interlimb interactions have also been demonstrated, e.g., in the form of effects of passive limb movements on the stability of rhythmic interlimb coordination (Serrien et al 2001;Stinear and Byblow 2001;Swinnen et al 1995).…”

Intralimb and Interlimb Incoordination: Comparative Study between Patients with Parkinsonism and with Cerebellar Ataxia

“…Characteristic wave forms for cluster 1 or 2 showed relatively preserved pattern of interlimb coordination that was characterized by coordinative movements of right and left pedals, while those for cluster 3 or 4 showed impaired pattern of interlimb coordination [3][4][5] . Six patients with parkinsonism classified into cluster 3 or 4.…”

“…These patterns, which included irregular and burst-like amplitude modulations with intermittent changes in the relative phase, correlated with the presence of the freezing phenomenon in patients with patients with parkinsonism. Asai et al suggested that these particular amplitude modulations could be viewed as a typical sign of chaotic behavior in nonlinear dynamical systems 3) . These may be characteristic features of interlimb coordination.…”

“…"Interlimb coordination" as coordination between the left and right limbs and use a term "intralimb coordination" as coordination among two or more joints in the same limb. A survey of the literature has led us to hypothesize that intralimb incoordination may be a key clinical feature of cerebellar ataxia patients 1) , and thus needs to be distinguished from "interlimb incoordination", which is typical of patients with parkinsonism [3][4][5] . To obtain the results reported here, we measured intralimb incoordination in patients with cerebellar ataxia by using an ergometer with left and right pedals that can be rotated independently, and compared it with interlimb incoordination in patients with parkinsonism.…”

A CPG synergy model for evaluation of human finger tapping movements

“…Calancie [9] and Dimitrijevic et al [10] described the performance of rhythmic movements when electric stimulation was applied to spinal cord injury victims at constant intervals. Against this background, rhythmic movements such as walking have been modeled based on a CPG [11], [12]. It should be noted that CPG models cannot express non-stationary features of movements such as rapid changes in rhythm, amplitude and velocity even if the relevant structure can be determined appropriately.…”