Abstract

In primates, multiple corticospinal projections from the sensorimotor cortex operate in concert to regulate voluntary action. We examined the soma distributions of all those corticospinal neuron populations projecting to different zones in the cervical and more caudal spinal segments in the macaque that are labeled with retrogradely transported fluorescent tracers; 2–4 differentiable dyes were injected into different sites in the cervical spinal cord of each of 11 monkeys. Lamina V of the cerebral cortex, in which all corticospinal neuron somas were located, was unfolded with computer assistance to form a flat surface, and local soma densities were displayed on this plane as contour and 3-D maps. At least nine discrete, somatotopically organized corticospinal projections were identified. Three separate corticospinal projections originated in frontal cortex. The first projected mostly from area 4 (≈35% of the total contralateral neuron population), but also from the adjacent dorsolateral area 6α (≈6% of total). The second large corticospinal projection (≈15% of total) originated in the supplementary motor area and a third small projection (≈2.6% of total) projected from the “postarcuate” cortex. Two separate corticospinal neuron populations were identified in areas 24 (≈6% of total) and 23 (≈4% of total) of the cingulate cortex. Thus, nearly 70% of the contralateral corticospinal projection originated in fromtal and cingulate cortex. At the boundary between the primary motor and somatosensory cortex there was a sharp change in the pattern of projections. Only ≈2.2% of the contralateral corticospinal projection originated in area 3a, rising to ≈9% in areas 3b/1, and ≈13% in areas 2/5. The projections from SII and insula totaled 3.4%. Ipsilateral and contralateral corticospinal projection patterns were similar, but the ipsilateral projection was only ≈8.1% of that from the contralateral cortex. Each corticospinal neuron population had terminals in the intermediate zone of all spinal segments; additionally, there were ventral horn projections from the primary motor and cingulate cortex, and dorsal horn projections from the somatosensory cortex.

Recognizing a number of separate populations of corticospinal neurons in the frontal, parietal, and insular cortex, each with unique thalamic and cortical inputs, and each of which has continuous access to all spinal motoneuron populations, underlines the importance of cortical and spinal connections linking them and coordinating their action. No coherent model of the cortical control of limb movements that incorporates this functional anatomy yet exists.

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