Manual dexterity: how does the cerebral cortex contribute?

Abstract

1. Manual dexterity, of great evolutionary significance to the primates, ranges in complexity from the precise opposition of finger and thumb to Brendal playing Mozart. All dexterity depends on a sustained and rapid transfer of sensorimotor information between the cerebral cortex and the cervical spinal cord. 2. Multiple separate corticospinal neuron populations originate from cortical areas four, the supplementary motor area, anterior cingulate, postarcuate, parietal and insular cortex. Each corticospinal neuron population projects in parallel to all spinal segments, and has a distinctive pattern of terminations. 3. Each corticospinal neuron population has a unique thalamic input which can relay particular sensorimotor information from the sense organs, cerebellum and basal ganglia. The overall structural framework of these sensorimotor pathways, with many parallel corticospinal channels, with interconnections in the cerebral cortex and spinal cord to enable crosstalk between the channels, is that needed for parallel distributed processing, which would enable the very rapid transfer of information between the cerebral cortex and spinal cord needed for any sophisticated use of the hand. 4. Hemisection of the cervical spinal cord in the macaque results in an immediate hemiplegia, with subsequent remarkable although incomplete recovery of hand and finger movements. The only direct corticospinal input to the hemicord caudal to the hemisection, even after 3 years, is the approximately 10% of fibres which cross the midline caudal to the lesion: the fibres 'spared' by the hemisection. A matching 'sparing' of somatosensory input from the paresed limb also occurs. No regeneration of the interrupted pathways has been visualized using modern tracer techniques. 5. Cervical hemisection permanently reduces the number of parallel channels which transmit information between cortex and spinal cord, but does not reduce their cortical origins nor the neuron populations targeted in the spinal cord. We infer that the content of the information that can be transmitted between the cortex and spinal cord is not greatly changed, but the rate of transmission of this information is sharply reduced, and is the 'bottleneck' that limits the complete recovery of dexterity following hemisection. The remarkable recovery that does occur presumably reflects more economic transmission of information by the few spared channels. We guess that this involves substantial synaptic reorganization not visualized by the procedures we have used.