Multiple Corticospinal Neuron Populations in the Macaque Monkey Are Specified by Their Unique Cortical Origins, Spinal Terminations, and Connections

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 (approximately 35% of the total contralateral neuron population), but also from the adjacent dorsolateral area 6a alpha (approximately 6% of total). The second large corticospinal projection (approximately 15% of total) originated in the supplementary motor area and a third small projection (approximately 2.6% of total) projected from the "postarcuate" cortex. Two separate corticospinal neuron populations were identified in areas 24 (approximately 6% of total) and 23 (approximately 4% of total) of the cingulate cortex. Thus, nearly 70% of the contralateral corticospinal projection originated in frontal and cingulate cortex. At the boundary between the primary motor and somatosensory cortex there was a sharp change in the pattern of projections. Only approximately 2.2% of the contralateral corticospinal projection originated in area 3a, rising to approximately 9% in areas 3b/1, and approximately 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 approximately 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.

Different Characteristics of the Corticospinal Tract According to the Cerebral Origin: DTI Study

“…10,[33][34][35] Several previous studies have reported the distribution of the CST origin in the cerebral cortex in primates. 11,12,14,17 In 1961,…”

“…[6][7][8][9][10] Many previous studies have reported differences in characteristics of CST fibers, in terms of the amount of CST fibers and function, according to the origin of the cerebral cortex. [11][12][13][14][15][16][17][18] Most of these studies have used animal brains because only postmortem histologic studies or microelectrode stimulation studies have been used for research on the human brain. 11,[14][15][16][17] By contrast, diffusion tensor tractography, a technique derived from DTI, allows 3D visualization and estimation of the CST.…”

“…[11][12][13][14][15][16][17][18] Most of these studies have used animal brains because only postmortem histologic studies or microelectrode stimulation studies have been used for research on the human brain. 11,[14][15][16][17] By contrast, diffusion tensor tractography, a technique derived from DTI, allows 3D visualization and estimation of the CST. [19][20][21] Several diffusion tensor tractography studies have reported the characteristics of the whole CST [22][23][24] ; however, little is known about differences in CST fibers according to the cerebral origin.…”

Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons.

“…However, it is not known which pathways mediate these motor effects. Compared with other premotor areas, corticospinal outputs from F5 are few in number and do not project as far as the cervical enlargement, where motor nuclei supplying hand muscles are located, but terminate at midcervical levels (He et al, 1993;Galea and Darian-Smith, 1994).…”

Organization of Multisynaptic Inputs from Prefrontal Cortex to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Rabies Virus

“…The primary motor cortex (MI), lying in the caudalmost portion of the lobe, has massive projections to the spinal cord in a strict somatotopic manner (He et al, 1993;Galea and Darian-Smith, 1994;Dum and Strick, 1996). This implies the involvement of the MI in the precise control of somatic movements (Georgopoulos et al, 1982;Kakei et al, 1999).…”