Abstract
The corticospinal (CS) tract emerged and evolved in mammals, and is essentially involved in voluntary movement. Over its phylogenesis, CS innervation gradually invaded to the ventral spinal cord, eventually making direct connections with spinal motoneurons (MNs) in higher primates. Despite its importance, our knowledge of the origin of the direct CS-MN connections is limited; in fact, there is controversy as to whether these connections occur in subprimate mammals, such as rodents. Here we studied the retrograde transsynaptic connection between cortical neurons and MNs in mice by labeling the cells with recombinant rabies virus. On postnatal day 14 (P14), we found that CS neurons make direct connections with cervical MNs innervating the forearm muscles. Direct connections were also detected electrophysiologically in whole cell recordings from identified MNs retrogradely-labeled from their target muscles and optogenetic CS stimulation. In contrast, few, if any, lumbar MNs innervating hindlimbs showed direct connections on P18. Moreover, the direct CS-MN connections observed on P14 were later eliminated. The transient CS-MN cells were distributed predominantly in the M1 and S1 areas. These findings provide insight into the ontogeny and phylogeny of the CS projection and appear to settle the controversy about direct CS-MN connections in subprimate mammals.
Highlights
The corticospinal (CS) tract is a phylogenetically novel descending pathway that emerged and evolved in mammals, culminating in the higher primates, and is centrally involved in voluntary movements[1,2]
We found that CS neurons make direct connections with cervical MNs innervating forearm muscles, but not lumbar MNs innervating hindlimbs, and that these direct CS-MN connections are present at an early stage of development, but are later eliminated during development
A mixture of G protein-deleted rabies virus expressing GFP (RV-ΔG-GFP), which is incompetent for transsynaptic spread[18,19,22] and adeno-associated virus (AAV) serotype 6 encoding the G protein and RFP, which lacks ability of transsynaptic spread alone was injected into the forearm muscles of mice on postnatal day (P) 5 to P7 (Fig. 1a)
Summary
The corticospinal (CS) tract is a phylogenetically novel descending pathway that emerged and evolved in mammals, culminating in the higher primates, and is centrally involved in voluntary movements[1,2]. We previously found that CS axons make direct synapses on MNs innervating distal forelimb muscles at an early stage of development in rats[12] and mice[13], which was shown by a different group, recently[14] Whether these direct CS-MN connections are transient or persist into adulthood is not yet clear, . We found that CS neurons make direct connections with cervical MNs innervating forearm muscles, but not lumbar MNs innervating hindlimbs, and that these direct CS-MN connections are present at an early stage of development, but are later eliminated during development These transient corticomotoneuronal (CM) cells predominantly were distributed in the M1 and S1 areas. These findings appear to settle the long-standing controversy about the direct CS-MN connections in subprimate mammals; they provide insight into the ontogeny and phylogeny of the CS projection
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