Reorganization of multi-muscle and joint withdrawal reflex during arm movements in post-stroke hemiparetic patients

Abstract

Objectives

To investigate the behavior of the nociceptive withdrawal reflex (NWR) in the upper limb during reaching and grasping movements in post-stroke hemiparetic patients.

Methods

Eight patients with chronic stroke and moderate motor deficits were included. An optoelectronic motion analysis system integrated with a surface EMG machine was used to record the kinematic and EMG data. The NWR was evoked through a painful electrical stimulation of the index finger during a movement which consisted of reaching out, picking up a cylinder, and returning it to the starting position.

Results

We found that: (i) the NWR is extensively rearranged in hemiparetic patients, who were found to present different kinematic and EMG reflex patterns with respect to controls; (ii) patients partially lose the ability to modulate the reflex in the different movement phases; (iii) the impairment of the reflex modulation occurs at single-muscle, single-joint and multi-joint level.

Conclusions

Patients with chronic and mild-moderate post-stroke motor deficits lose the ability to modulate the NWR dynamically according to the movement variables at individual as well as at multi-muscle and joint levels.

Significance

The central nervous system is unable to use the NWR substrate dynamically and flexibly in order to select the muscle synergies needed to govern the spatio–temporal interaction among joints.

Introduction

Reaching and grasping arm movements with the affected limb in hemiparetic patients are characterized by decreased movement speed, lack of smoothness and coordination, and abnormal patterns of muscle activation (Hammond et al., 1988, Gowland et al., 1992, Trombly, 1992). This motor impairment is due mainly to disruption of the planning and execution of reaching and precision grasping due to primary motor cortex or corticospinal tract damage, as has been extensively observed in primates and humans (Hepp-Reymond and Wiesendanger, 1972, Maier et al., 1993, Aruin, 2005, Gölge et al., 2004, Grichting et al., 2000, Muir and Lemon, 1983, Nowak et al., 2003, Beer et al., 2000, Takahashi and Reinkensmeyer, 2003, Quaney et al., 2005, Wenzelburger et al., 2005, Raghavan et al., 2006).

However, the spinal contribution to abnormal patterns of movement following stroke has not been well investigated. Spasticity and deficits in voluntary control of movement are both, in some way, related to disorders in the organization of segmental reflex activity (e.g. Corcos et al., 1986, Powers et al., 1988, Levin and Feldman, 1994). During reaching tasks, a relationship has been observed between an impaired voluntary range of movement and limitations in the range of stretch reflex regulation at individual muscle level (Levin and Feldman, 1994, Levin et al., 2000). Although a number of studies have focused on changes occurring in monosynaptic reflexes in a single-joint following stroke (Thilmann and Fellows, 1991, Wilson et al., 1999, Condliffe et al., 2005), there is a lack of research addressing the role of polysynaptic multi-joint reflexes. Thus, it is not known how these reflexes in the upper extremities are modulated during movement in stroke survivors compared to healthy subjects.

In a general motor context, control systems exploit reflexes in movement and force or torque production, which is consistent with the fact that reflexes are broadly adjustable rather than rigid stimulus–response constructs (Balasubramaniam and Feldman, 2004). Spinal reflex pathways acting at multi-joint levels may be activated by descending commands to generate and coordinate voluntary movements (Lundberg, 1979).

The few studies that have investigated upper limb polysynaptic reflexes in stroke patients were performed only at rest (Dewald et al., 1999), during either passive (Black et al., 2007) or active, but machinery constrained, arm movements (Sangani et al., 2007). It would, however, be useful to investigate simultaneously the spinal reflexes in several muscles during unconstrained natural arm movements in order to obtain a global picture of spinal function and its modulation.

Of the various polysynaptic spinal reflexes, the withdrawal reflex has been proved to be a useful tool for investigating changes in spinal cord function during lower limb movements in humans (Crenna and Frigo, 1984, Duysens et al., 1990, Duysens et al., 1992, Rossi and Decchi, 1994, Andersen et al., 1995, Andersen, 2007, Spaich et al., 2004, Spaich et al., 2006, Sandrini et al., 2005, Emborg et al., 2009), given that these changes are due to converging inputs from the peripheral afferents and descending motor commands to the spinal cord neurons (Baldissera et al., 1981).

Although the flexion synergy evoked by painful stimuli serves a primarily protective function, various studies have shown that the nociceptive withdrawal reflex (NWR) also fulfills a more complex motor function (for a review see Sandrini et al., 2005).

A few years ago (Serrao et al., 2006), we investigated the modulation of the NWR in human upper limbs during reaching and grasping movements performed freely in three-dimensional space. We found that the NWR undergoes state- and phase-dependent modulation according to the mechanical function exerted by each muscle in the course of the motor sequence. In particular, we observed that the amount and direction of the motion occurring at each joint in the course of the motor task were the main factors determining the presence of either reflex reversal (presence of the reflex in either agonist or antagonist muscle in a phase reversal manner) or co-presence (presence of the reflex in both antagonist muscles without phase reversal) patterns (Serrao et al., 2006). These findings suggest that transmission along the excitatory reflex pathways is highly adaptable to the motor context and related to the joint motion, and that supraspinal centers possibly exploit the same interneuronal spinal network in order to regulate voluntary movements and reflex responses in a complex, multisegmental way.

Application of this method in hemiparetic stroke survivors may help to further understanding of the role of the descending pathways in dynamically recruited spinal neurons (both motorneurons and interneurons) involved in mediating reflexes, and also shed light on the reorganization processes and adaptive changes occurring at multi-segmental level in the spinal cord.

We set out to investigate the behavior of the NWR in terms of kinematic and EMG responses following electrical painful stimulations during reaching and grasping movements in the upper limb in a sample of post-stroke hemiparetic patients.