RAPID COMMUNICATION Changes in the Temporal Pattern of Primary Motor Cortex Activity in a Directional Isometric Force Versus Limb Movement Task

Sergio, Lauren E. and John F. Kalaska. Changes in the temporal correlated with other spatial kinematic parameters of handpattern of primary motor cortex activity in a directional isometric paths, including the direction and velocity of hand movement force versus limb movement task. J. Neurophysiol. 80: 1577– and target distance (Ashe and Georgopoulos 1994; Fu et al. 1583, 1998. We recorded the activity of 75 proximal-arm-related 1995; Georgopoulos et al. 1982; Kalaska et al. 1989; cells in caudal primary motor cortex (MI) while a monkey generSchwartz 1992; Schwartz et al. 1988). Therefore published ated either isometric forces or limb movements against an inertial studies to date would appear to suggest that the representaload. The forces and movements were in eight directions in a tion of motor actions in MI is better correlated with task horizontal plane. The isometric force generated at the hand inkinetics under isometric conditions and with task kinematics creased monotonically in the direction of the target force level. under movement conditions. However, the validity of this The force exerted against the load in the movement task was more complex, including a transient decelerative phase during the moveapparent task dependence has not been confirmed experiment as the hand approached the target. Electromyographic (EMG) mentally. No study has compared the activity of the same activity of proximal-arm muscles reflected the task-dependent MI cells during both whole-limb isometric and reaching changes in dynamics, showing a ramp increase in activity during tasks with similar spatial ( i.e., directional) behavioral conthe isometric task and a reciprocal triphasic burst pattern in the straints and with direct measures of the output forces at the movement task. A sliding 50-ms window analysis showed that the hand. The present study attempts to fill this void. directionality of the EMG, when expressed in hand-centered spatial coordinates, remained stable throughout the isometric ramp but often showed a significant transient shift during the limb moveM E T H O D S ments. Many cells in M1 showed corresponding significant changes in activity pattern and instantaneous directionality between the two A juvenile male rhesus monkey (Macaca mulatta , 5 kg) was tasks. This momentary dissociation of discharge from the directrained to perform both an isometric force task and a limb-movetional kinematics of hand displacement is evidence that the activity ment task against an inertial load. The isometric force task is of many single proximal-arm related M1 cells is not coupled only described elsewhere (Sergio and Kalaska 1997). Briefly, the anito the direction and velocity of hand motion. mal exerted a force with its right arm against a handle attached to a 6-df force/ torque transducer (Assurance Technologies, F3/T10 system) placed in front of him. In the movement task, an identical I N T R O D U C T I O N handle/force transducer assembly was housed in the base of a 1.6m long weighted pendulum. The weight of the transducer assembly Many studies showed that primary motor cortex (MI) cell was 1,300 g, and that of the pendulum plus transducer was 2,600 g. activity is often correlated to parameters of task dynamics An emitter attached to the pendulum base allowed a sonic digitizer or kinetics under isometric conditions in single-joint tasks (Science Accessories, model GP-9) to measure the x-y position of (Ashe 1997; Cheney and Fetz 1980; Evarts 1969; Humphrey the base at 55 Hz with 0.1-mm resolution. The monkey’s starting and Tanji 1991) and in whole arm tasks (Ashe 1997; Georhand location in the movement task was identical to that in the gopoulos et al. 1992; Sergio and Kalaska 1997; Taira et al. isometric task. A computer monitor was positioned at eye level 60 cm in front 1996). Similarly, the covariation of discharge of many MI of the monkey. In the isometric task, a cursor displayed on the cells with the direction of external loads acting on the arm monitor gave continuous feedback corresponding to the current during reaching movements (Kalaska et al. 1989) suggests force level applied to the force transducer in the x-y (horizontal) that kinetic parameters of motor output are also represented plane. At the start of each trial, a circle appeared at the center of in MI during reaching. If so, the laws of motion predict that the monitor, and the monkey generated a small static force (0.3 movement-related cell activity should show a good relation N) away from its body to position the cursor within the central to the time course of hand acceleration. However, the only force target for a variable period of time (1–3 s) . The central study to test this prediction during reaching found only modtarget then disappeared, and one of eight peripheral force targets est correlations with acceleration (Ashe and Georgopoulos (0.28 N diam) arrayed in a circle around the central target appeared. 1994). In contrast, MI single-cell activity was frequently The separation of the centers of the central and peripheral targets corresponded to a 1.5 N change of force. The monkey generated a force ramp in the indicated direction to displace the cursor into The costs of publication of this article were defrayed in part by the the peripheral target and hold it there for 2 s. Target directions payment of page charges. The article must therefore be hereby marked were spaced at 457 intervals, starting from 07 (directly to the right) ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. and rotating counterclockwise. The eight targets were repeated five