Mouse corticospinal system comprises different functional neuronal ensembles depending on their hodology

Abstract

Background Movement performance depends on the synaptic interactions generated by coherent parallel sensorimotor cortical outputs to different downstream targets. The major outputs of the neocortex to subcortical structures are driven by pyramidal tract neurons (PTNs) located in layer 5B. One of the main targets of PTNs is the spinal cord through the corticospinal (CS) system, which is formed by a complex collection of distinct CS circuits. However, little is known about intracortical synaptic interactions that originate CS commands and how different populations of CS neurons are functionally organized. To further understand the functional organization of the CS system, we analyzed the activity of unambiguously identified CS neurons projecting to different zones of the same spinal cord segment using two-photon calcium imaging and retrograde neuronal tracers. Results Sensorimotor cortex slices obtained from transgenic mice expressing GCaMP6 funder the Thy1 promoter were used to analyze the spontaneous calcium transients in layer 5 pyramidal neurons. Distinct subgroups of CS neurons projecting to dorsal horn and ventral areas of the same segment show more synchronous activity between them than with other subgroups. Conclusions The results indicate that CS neurons projecting to different spinal cord zones segregated into functional ensembles depending on their hodology, suggesting that a modular organization of CS outputs controls sensorimotor behaviors in a coordinated manner.

Corticospinal neurons from motor and somatosensory cortices exhibit different temporal activity dynamics during motor learning

“…Here, we describe in the mouse that CSp neurons projecting to the cervical spinal cord are anatomically broadly distributed in the contralateral cortex including motor (M1 and M2) and somatosensory (S1 and S2) cortices. It has been shown that different groups of CSp neurons project, in a segregated manner, to the same segment of the spinal cord in rats (Olivares-Moreno et al, 2017), mice (Asante and Martin, 2013;Kameda et al, 2019;Olivares-Moreno et al, 2019;Steward et al, 2021) and monkeys (Coulter and Jones, 1977). These studies show that CSp tract projections from M1 conspicuously avoid the dorsal horn, while S1 projections preferentially terminate into the dorsal horn.…”

Corticospinal populations broadcast complex motor signals to coordinated spinal and striatal circuits

“…Corticospinal output is topographically organized: CSNs within regions that control specific body parts preferentially innervate spinal segments containing the circuits that control the muscles for those body parts 2 , 3 , 5 – 7 . CSNs arising from motor regions of isocortex form synapses spread across intermediate and ventral laminae of the spinal grey, home to premotor spinal interneurons; while sensory cortical CSNs have terminal fields mostly restricted to superficial regions of spinal cord, home to the dorsal horn interneurons that regulate peripheral sensory feedback 8 , 9 . Partly because of this anatomy, motor cortical CSNs have been hypothesized to control the activity of individual muscles or muscle synergies through their direct projections to the spinal cord 10 – 12 .…”

Motor Cortex Projections To Red Nucleus And Pons Have Distinct Functional Roles In The Mouse

“…We provided functional, anatomical, and morphological evidence indicating that two distinct populations of PTNs differentially contribute to motor execution. Previous studies have described the relationships between structure and function in Layer 5 PTNs projecting to different targets (Groh et al, 2010; Rojas-Piloni et al, 2017; Olivares-Moreno et al, 2019). Our data revealed that both classes of PTNs are intermingled in sensorimotor cortices, including M1, and only a small proportion of neurons seem to contact the RN and PN simultaneously.…”