Coordination of axial rotation and step execution: deficits in Parkinson's disease

Abstract

To determine why parkinsonian patients (PP) present some difficulties to initiate locomotion, a diagonal step has been investigated in two tasks in five control subjects (CS) and in ten PP. In the first task, the subjects had to perform one diagonal step without change in their orientation (WR); in the second task, they had to perform one diagonal step with a body rotation in the step direction (RO). The defended hypothesis is that the gait initiation deficits in Parkinson disease are a consequence of their difficulties to coordinate al the component of a complex movement. The analysed parameters were the duration of the postural and movement phases, the step length and velocity, and the amplitude of the horizontal ground reaction forces during each phase. Compared to CS, the PP showed a lengthening of the postural phase, a decrease in the step length and velocity and a reduction of the horizontal forces. The comparisons between the performances obtained in the WR versus those obtained the RO show in CS that the performances remained unchanged, whereas in PP the performances were significantly more altered in the RO. It illustrates the specific deficit occurring in PP while performing complex tasks where coordination between several components has to be achieved simultaneously.

Introduction

The mechanisms involved in gait initiation of control subjects (CS) have been previously studied by performing kinetic and electromyographic recordings (EMG) [1] and more recently by kinematics, kinetics and EMG data [2]. The gait initiation process can be described as a succession of two phases: the postural phase and the stepping (or movement) phase [3], [4]. These two phases would correspond to two coordinated motor commands that are presumed to act mainly on the distal leg muscles [5]. Indeed, the onset of the postural phase corresponds to the generation of propulsive forces [3]. During the postural phase, the center of pression (COP) is moved posteriorly and towards the moving leg, thus accelerating the center of gravity (CG) forward and towards the postural leg [6]. The Backward COP displacement results from a deactivation of the gastrocnemii and soleus muscles and the lateral displacement of the COP is the consequence of a momentary loading of the movement leg by the hip abductors [6]. The CG shift allows the first step to be initiated by a second motor command acting on the plantarflexors of the stepping leg contributing to the heel lift-off. Thus, the gait initiation process requires coordination between the ongoing whole body postural preparation, which corresponds to the CG shift forward and laterally, and the leg movement, which corresponds to the first step execution. Both motor commands have to be tightly coordinated possibly using on proprioceptive [7] or cutaneous [8] information related to the CG shift.

In Parkinson's disease, the gait initiation disorders become obvious when the patients start suffering from postural instability, which progressively appears in the later stages of the disease. On physical examination, the gait initiation impairment, also called ‘slipping clutch phenomenon’ [9], can be aggravated to such an extent that the patient becomes ‘frozen to the spot’ [10], [11] or ‘suddenly blocked’ [12]. These freezing episodes suggest that the impairment of postural phase could reach a stage beyond which the step triggering would become no longer possible. This disabling problem explains why considerable attention has been recently focused on the gait initiation impairments in Parkinson's disease and related disorders [13], [14], [15]. Using combined kinematic, kinetic and EMG analysis, Crenna et al. [16] have previously shown that the main abnormality observed during gait initiation in Parkinson's disease consisted of an increased duration of the postural phase and a decrease in propulsive forces during postural and movement phases. As a result, the step length was shorter and the step velocity was slower. These data have been confirmed in recent studies [4], [14].

To explain these observations, two complementary hypotheses have been put forward. In the first one, the deficit in propulsive forces would be restricted to the postural preparation preceding and accompanying the first step. In the second hypothesis, the main deficit would concern the coordination between the postural preparation and the triggering of the first step [17], [4], [5]. It is well established in Parkinson's disease that the freezing episodes become more obvious when a directional change occurs during gait [18], [19]. It can be expected that the postural preparation becomes more complex when it comprises not only the body's inclination forward and onto the supporting leg but also the whole body re-orientation in the step direction. This re-orientation corresponds to an axial rotation of different body segments, namely the head and the trunk (shoulders and pelvis). Because of their difficulty to coordinate two tasks simultaneously [20], or sequentially [21], any directional change during gait should stress the step initiation impairments in parkinsonian patients (PP).

In this framework, we investigated the influence of a supplementary postural constraint (i.e. change in whole body orientation) on the process of postural preparation accompanying a single diagonal step (45° forward and side ways). The question raised was: does body re-orientation, simultaneously required during postural preparation, increase the impairment of diagonal step performances in Parkinson's disease? To answer this question, a diagonal step initiation without any change in the whole body orientation was taken as a reference condition. The hypothesis was that in control subject the simultaneous postural preparation and rotation of the body would not influence the diagonal step performance. On the contrary, the incapacity of PP to coordinate different components of a complex movement would aggravate strongly their disorders in gait initiation.