Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching
Introduction
Reaching movements provide an ideal paradigm for understanding how sensory information is converted into coordinated motor behavior. On the sensory side, movements to spatial targets require the integration of visual and proprioceptive information to select and plan the impending limb movement. On the motor side, force generated by a muscle generates motion at both spanned and non-spanned joints due to intersegmental dynamics (Hollerbach and Flash, 1982, Zajac and Gordon, 1989). This coupling between shoulder and elbow muscle activity and motion requires the CNS to carefully coordinate the motor patterns of muscles at these joints in order to smoothly move the hand in space.
Visually guided reaching movements by monkeys has become an important paradigm to study how regions of the brain, such as primary motor cortex (MI), are involved in the planning and control of voluntary movement (Kalaska and Crammond, 1992, Georgopoulos, 1995, Shen and Alexander, 1997, Zhang et al., 1997). In spite of many years of research, lively debate still remains on the most appropriate way for interpreting the discharge patterns of individual cells in MI. On the one side, many studies have illustrated that the discharge pattern of individual cells are broadly tuned to the direction of hand movement and that a population vector, constructed from the discharge patterns of a large sample of cells, tends to point in the direction of movement (Georgopoulos et al., 1988, Schwartz et al., 1988, Schwartz, 1994). The implication from these studies is that individual cells in MI may be related to higher level features of movement related to the global goal of the task such as the direction of hand movement. On the other side, the discharge of individual cells has been found to share common temporal and spatial features with the activity patterns of proximal arm muscles during reaching (Murphy et al., 1985, Miller et al., 1996, Scott, 1997) suggesting that MI may be involved in the details of motor output at the shoulder and elbow joints.
It seems surprising that such divergent frameworks for interpreting the neural representation in MI during reaching movements are espoused in the literature. However, the ability to find neural correlates of movement to support these different views at least partially reflects the inherent coupling between different variables of movement (Mussa-Ivaldi, 1988, Scott and Kalaska, 1997). Extrinsic variables of movement, such as the kinematics of the hand, covary with intrinsic variables, such as motion of the shoulder or the activity of proximal arm muscles. As a result, neural activity related to a specific feature of movement will also covary with many other variables.
In order to dissociate the various parameters of movement, several studies have examined the response patterns of individual cells when reaching movements are performed under different mechanical loads or arm postures (Kalaska et al., 1989, Caminiti et al., 1990, Scott and Kalaska, 1997). A consistent finding from these studies is that the directional tuning of many MI cells are modified by load or posture. These results suggest that the activity of cells is not simply related to the direction of hand movement, but may be at least partially related to intrinsic features of the task, such as joint kinematics or kinetics. However, further progress on interpreting the nature of the discharge patterns of these cells based on features of motor execution are difficult in these studies because neural activity was only related to hand position or motion.
The major stumbling block for identifying the nature of the neural representation in MI during reaching is the difficulty of quantifying and manipulating the mechanics of multi-joint motion. The present article describes a new device developed specifically to address this problem called KINARM (kinesiological instrument for normal and altered reaching movements). The device uses a four-bar linkage and torque motors to record the motion of the arm in the horizontal plane and apply loads to each joint independently. While related devices have been developed to apply loads to the arm during multi-joint movements (Shadmehr and Mussa-Ivaldi, 1994, Gomi and Kawato, 1996), the loads have always been applied through the hand. A unique feature in the present system is that the loads are applied directly to the upper arm and forearm and allow the loads to be focused either at the shoulder or elbow joints, or both.
Section snippets
Methods
KINARM is an exoskeleton that attaches to the upper arm and forearm of a monkey (Fig. 1). The mechanical linkage allows the monkey to make combined flexion and extension movements of the shoulder and elbow joints to move its hand to targets in the horizontal plane. The linkage is adjustable to align its ball-bearing joints with the centers of rotation of the shoulder and elbow joints. Custom-made fibre-glass braces covered with a closed-cell foam provide an interface between the mechanical
Results
One juvenile male monkey (6.5 kg) has been trained to wear KINARM and perform a variety of multi-joint motor tasks, including reaching movements with and without viscous loads, as well as postural tasks when intermittent or constant torque loads are applied by the device. Fig. 3 illustrates the net muscular torque at the shoulder and elbow for repeated trials in which the monkey was trained to maintain its hand at a central target while different loads were applied by the motors. A load applied
Discussion
Visually guided reaching movements have become an important paradigm for studying how regions of the brain, such as primary motor cortex, are involved in planning and controlling movement (Kalaska and Crammond, 1992, Georgopoulos, 1995). These multi-joint tasks require visual information to be converted into motor patterns at the shoulder and elbow joints to move the hand through space. Due to the difficulties of monitoring the kinematics of multi-joint motion, a common approach for
Nomenclature
c distance from center of mass to proximal end of segment/link d, g, h static and dynamic friction constants f contact force on link 5 f′ contact force on link 4 I moment of inertia l length of a segment/link m mass of a segment/link T Torque Angular position, velocity and acceleration 1–5 segment/links 1–5 e elbow joint of monkey s shoulder joint of monkey m1 motor 1 m2 motor 2 x, y cartesian coordinates (local) X, Y cartesian coordinates (global)
Acknowledgements
The author would like to thank a number of people that facilitated the completion of this facility; Gaetan Richard and Jacques Berichon at the Université de Montréal for drafting and machining the mechanical device, Paul Cisek for the development of software to display the kinematics and kinetics of movement, Kim Moore and Marie-Josiée Bourque for expert technical support, and Jerry Loeb and the BMEU at Queen’s University for the fibre-glass arm braces and various electronic components for data
References (26)
Current issues in directional motor control
Trends Neurosci
(1995)Do neurons in the motor cortex encode movement direction? An alternative hypothesis
Neurosci Lett
(1988)- et al.
Making arm movements within different parts of space: dynamic aspects in the primate motor cortex
J Neurosci
(1990) - et al.
Cooperative action for mono- and bi-articular arm muscles during multi-joint posture and movement tasks in monkeys
Soc Neurosci Abstr
(1998) - et al.
Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population
J Neurosci
(1988) - et al.
Equilibrium-point control hypothesis examined by measured arm stiffness during multijoint movement
Science
(1996) - et al.
Temporal and amplitude generalization in motor learning
J Neurophysiol
(1998) - et al.
Dynamic interactions between limb segments during planar arm movement
Biol Cybern
(1982) - et al.
Cerebral cortical mechanisms of reaching movements
Science
(1992) - et al.
A comparison of movement direction-related versus load direction-related activity in primate motor cortex, using a two-dimensional reaching task
J Neurosci
(1989)
Timing and magnitude of electromyographic activity for two-joint arm movements in different directions
J Neurophysiol
Rapid adaptation to coriolis force perturbations of arm trajectory
J Neurophysiol
A muscle-space description of motor cortical discharge
Soc Neurosci Abstr
Cited by (258)
Towards a unified neural mechanism for reactive adaptive behaviour
2021, Progress in NeurobiologyImpaired proprioception and magnified scaling of proprioceptive error responses in chronic stroke
2024, Journal of NeuroEngineering and RehabilitationA robot-based interception task to quantify upper limb impairments in proprioceptive and visual feedback after stroke
2023, Journal of NeuroEngineering and Rehabilitation