Terminal distribution of the corticospinal projection from the hand/arm region of the primary motor cortex to the cervical enlargement in rhesus monkey

Abstract

To further our understanding of the corticospinal projection (CSP) from the hand/arm representation of the primary motor cortex (M1), high-resolution anterograde tracing methodology and stereology were used to investigate the terminal distribution of this connection at spinal levels C5 to T1. The highest number of labeled terminal boutons occurred contralaterally (98%) with few ipsilaterally (2%). Contralaterally, labeled boutons were located within laminae I – X, with the densest distribution found in lamina VII and, to a lesser extent, laminae IX and VI. Fewer terminals were found in other contralateral laminae. Within lamina VII, terminal boutons were most prominent in the dorsomedial, dorsolateral and ventrolateral subsectors. Within lamina IX, the heaviest terminal labeling was distributed dorsally. Ipsilaterally, boutons were found in laminae V – X. The most pronounced distribution occurred in the dorsomedial and ventromedial sectors of lamina VII and fewer labeled boutons were located in other ipsilateral laminae. Segmentally, contralateral lamina VII labeling was highest at levels C5-C7. In contrast, lamina IX labeling was highest at C7-T1 and more widely dispersed amongst the quadrants at C8-T1. Our findings suggest dominant contralateral influence of the M1 hand/arm CSP, a contralateral innervation pattern in lamina VII supporting Kuypers (1982) conceptual framework of a “lateral motor system”, and a projection to lamina IX indicating significant influence on motoneurons innervating flexors acting on the shoulder and elbow rostrally (C5-C7), along with flexors, extensors, abductors and adductors acting on the digits, hand and wrist caudally (C8-T1).

Histological and electrophysiological analysis of the corticospinal pathway to forelimb motoneurons in common marmosets

“…This remarkable bilaterality of the CST projection is quantitatively distinct from observations in rats (Rouiller et al, 1991;Brus-Ramer et al, 2007). In contrast, the anatomy revealed in the present study is similar to the CST organization of the Old World monkey (Rosenzweig et al, 2009;Yoshino-Saito et al, 2010;Morecraft et al, 2013) and of humans (Nathan et al, 1990). Furthermore, in this study, we observed the spiking response of spinal neurons induced by repetitive CST stimulation on laminae VII-VIII of the spinal gray matter ipsilateral to the pyramidal stimulation with relatively short segmental latency (1.8 ms), which suggested oligosynaptic linkage from the CST.…”

“…For the latter purpose, excitatory and/or inhibitory synaptic responses evoked by electrical stimulation at the pyramid were recorded from spinal gray matter (field potentials) and motoneurons (intracellular recordings) at the lower cervical level. Bilateral projections from one hemisphere have been reported in other primate species (Rosenzweig et al, 2009;Yoshino-Saito et al, 2010;Morecraft et al, 2013), in which they might provide neural substrate for some recovery after spinal cord injury (Rosenzweig et al, 2010). Therefore, we also characterized the distribution of CST axons and synaptic responses of CST stimulation at different laminae on both sides of the spinal cord.…”

Preclinical and Clinical Evidence on Ipsilateral Corticospinal Projections: Implication for Motor Recovery

“…2) [3, 14, 39–41]. Interestingly, evidence for the crossing of ipsilateral fibers at spinal levels was also observed in multiple studies [3, 39, 40]; therefore, the presence of ipsilateral fibers suggested by BDA only indicates that these fibers descend ipsilaterally and there is a high likelihood that these fibers will re-cross and end up innervating contralateral neurons.…”

“…When the termination patterns of these ipsilateral fibers were assessed, they were found to cover spinal laminae V–IX, with the highest density (~80%) of innervation in ipsilateral lamina VIII, and very sparse termination in ipsilateral lamina IX (Table 2, Fig. 2) [3, 14, 39–41]. The consistent finding that the majority of iCST fibers terminate at lamina VIII challenges the functional significance of iCST fibers since lamina VIII mainly harbors commissural interneurons that project through the midline to the contralateral cord, thus largely contributing to contralateral movement control [46].…”

Cortical innervation of the hypoglossal nucleus in the non‐human primate (Macaca mulatta)

“…In selected cases, electrophysiological microstimulation was used in combination with ketamine (10 mg/kg) and diazepam (1.0 mg/kg) to map M1, LPMC and M2 which has been described in detail in our previous reports (McNeal et al, 2010; Morecraft et al, 2007a, 2013a). Briefly, stimulation was performed using a Grass Square Pulse Stimulator system (model S28; Grass Technologies, West Warwick, RI) with an attached tungsten electrode (impedance 0.5–1.5 MΩ).…”