Manual dexterity and corticospinal connectivity following unilateral section of the cervical spinal cord in the macaque monkey

The macaque recovers quite rapidly from the immediate severe flaccid hemiparesis that results from unilateral section of the cervical spinal cord (between C3 and C6) and starts to use the impaired hand to pick up objects within about 30 days following the surgery. Within another 60 days, the monkey is quite dexterous; nonetheless, there is a persisting deficit. We used video recording to study the long-term recovery of manual dexterity following unilateral section of the cervical cord in newborn and juvenile monkeys. A reach-and-retrieve manual task was examined. By using a preset oppositional force, opposition of the pads of the index finger and thumb in the vertical plane was needed to retrieve the desired target object. The corticospinal connectivity of each monkey was also examined by using retrograde or anterograde tracers at the end of the experimental period (Galea and Darian-Smith 1997 J. Comp. Neurol., this issue) and was correlated with the manual performance. Manually retrieving an object depends on the coordination of several control processes acting in parallel, including 1) visually guided components, such as directing the arm toward the object, aligning the digits with the target object by pronating the forearm, and preshaping the index/thumb separation to match with the size and shape of the target, and 2) manipulative components that depend on tactual input and that also include independent movements of the digits and the application of the appropriate oppositional forces. The impairment of manual dexterity that persisted after a cervical section, although it was small, involved these processes and was evident in 1) the less direct trajectory used in reaching, 2) the loss of preshaping of the separated index finger and thumb prior to grasping the target object, and 3) a weakening of the oppositional forces that could be developed between the pads of the index finger and thumb. Although, in the accompanying paper, we did not preclude some regeneration of severed corticospinal connections, we did show that, if any such reconstruction occurred, then it was limited. The remarkable but incomplete recovery of dexterity over a period of 6-12 months, therefore, must be achieved by 1) optimizing the transmission of information from the cortex to the spinal cord by the substantially reduced populations of corticospinal neurons and corticobulbospinal projections and/or 2) the effective use of spinal circuitry in regulating the more stereotyped elements of the manual task.