Dense projection of Stilling’s nucleus spinocerebellar axons that convey tail proprioception to the midline area in lobule VIII of the mouse cerebellum

Luo, Yuanjun; Onozato, Takeru; Wu, Xuanjing; Sasamura, Kazuma; Sakimura, Kenji; Sugihara, Izumi

doi:10.1007/s00429-020-02025-6

Cited by 16 publications

(12 citation statements)

References 46 publications

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“…Notably, localized stimulation of the ventral fastigial nucleus evokes increases in blood pressure ( Doba and Reis, 1972 ), and chemosensitive neurons responsive to CO 2 are similarly localized ventrally ( Martino et al, 2007 ), consistent with a role for F3 fastigial neurons in cardiovascular and respiratory responses to head tilt ( Woodring et al, 1997 ; Yates et al, 2002 ; Wilson et al, 2006 ) and hypercapnia ( Xu and Frazier, 2002 ). PCs in the F3 module extend over cerebellar cortical midline regions that receive vestibular and proprioceptive signals related to head and body position with respect to gravity ( Laurens et al, 2013 ; Luo et al, 2020 ). The F3 region of the medial accessory olive (cMAO-a) receives inputs from the lumbosacral spinal cord ( Molinari, 1985 ; Matsushita et al, 1992 ) and from cardiorespiratory regions of the nucleus tractus solitarius ( Loewy and Burton, 1978 ).…”

Section: Discussionmentioning

confidence: 99%

Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis

Fujita

Kodama

2020

eLife

190

264

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The cerebellar vermis, long associated with axial motor control, has been implicated in a surprising range of neuropsychiatric disorders and cognitive and affective functions. Remarkably little is known, however, about the specific cell types and neural circuits responsible for these diverse functions. Here, using single-cell gene expression profiling and anatomical circuit analyses of vermis output neurons in the mouse fastigial (medial cerebellar) nucleus, we identify five major classes of glutamatergic projection neurons distinguished by gene expression, morphology, distribution, and input-output connectivity. Each fastigial cell type is connected with a specific set of Purkinje cells and inferior olive neurons and in turn innervates a distinct collection of downstream targets. Transsynaptic tracing indicates extensive disynaptic links with cognitive, affective, and motor forebrain circuits. These results indicate that diverse cerebellar vermis functions could be mediated by modular synaptic connections of distinct fastigial cell types with posturomotor, oromotor, positional-autonomic, orienting, and vigilance circuits.

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Section: Discussionmentioning

confidence: 99%

Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis

Fujita

Kodama

2020

eLife

190

264

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“…In this study, we reconstructed single lumbar spinocerebellar axons labeled by localized injection of biotinylated dextran amine (BDA) and mapped their mossy fiber termination on the immunostained striped-compartmentalization pattern of aldolase C (zebrin II) expression in the cerebellum (Brochu et al, 1990;Fujita et al, 2014) in the mouse. The results were then compared with those of studies on thoracic spinocerebellar axons (Luo et al, 2018) and other cerebellar mossy fiber axons (Ando et al, 2020;Biswas et al, 2019;Luo et al, 2020;Quy et al, 2011) to distinguish the different types of projections and their functional and morphological significance.…”

Section: Antibody Namementioning

confidence: 99%

“…Seven adult male and female heterozygous Aldoc-Venus:C57BL/6N mice (Fujita et al, 2014) were used in retrograde labeling experiments. The samples analyzed here are the same as those used in our analysis of the sacral spinal cord (Luo et al, 2020). Methods of retrograde labeling of spinocerebellar neurons and their mapping have been described (Luo et al, 2020).…”

Section: Retrograde Labeling Of Spinocerebellar Axonsmentioning

confidence: 99%

“…Our single axon tracing study has shown that the three groups of thoracic spinocerebellar projections (non-crossed Clarke's column projection, NCC; noncrossed marginal Clarke's column projection, NMCC; and crossed medial ventral horn projection, CMVH) have distinct single axon morphologies, in the pathway, branching, and termination in the cerebellar lobules, indicative of different functional significances (Luo et al, 2018). We have used the same approach to characterize the sacral spinocerebellar projection (Luo et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Single axonal morphology reveals high heterogeneity in spinocerebellar axons originating from the lumbar spinal cord in the mouse

Zhang

Luo

Sasamura

et al. 2021

J of Comparative Neurology

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Among the spinocerebellar projections vital for sensorimotor coordination of limbs and the trunk, the morphology of spinocerebellar axons originating from the lumbar cord has not been well characterized compared to those from thoracic and sacral cords. We reconstructed 26 single spinocerebellar axons labeled by biotinylated dextran injections into the gray matter of the lumbar spinal cord in mice. Axon terminals were mapped with the zebrin pattern of the cerebellar cortex. Reconstructed axons were primarily classified into ipsilaterally and contralaterally ascending axons, arising mainly from the dorsal and ventral horns, respectively. The majority of ipsilateral and contralateral axons took the dorsal-medullary and ventral-pontine pathways, respectively. The axons of both groups terminated mainly in the vermal and medial paravermal areas of lobules II-V and VIII-IXa, often bilaterally but predominantly ipsilateral to the axonal origin, with a weak preference to particular portions of zebrin stripes. The ipsilateral axons originating from the medial dorsal horn in the upper lumbar cord (n = 3) had abundant (43-147) mossy fiber terminals and no medullary collaterals. The ipsilateral axons originating from the lateral dorsal horn in the lower lumbar cord (n = 9) and the contralateral axons (n = 14) showed remarkable morphology variations. The number of their mossy fiber terminals varied from 2 to 172. Their collaterals, observed in 17 axons out of 23, terminated mainly in the medial cerebellar nucleus, nucleus X, and lateral reticular nucleus in various degrees. The results indicated that the lumbar spinocerebellar projection contains highly heterogeneous axonal populations regarding their pathway, branching, and termination patterns.

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“…The mossy fiber projection, which is the main source of afferent axons to the cerebellar cortex, is not as tightly linked to PC compartments as PC axons or olivocerebellar axons (Quy et al, 2011;Biswas et al, 2019;Luo et al 2020). However, because early mossy fibers initially target PCs (Kalinovsky et al, 2011), the early PC cluster organization may affect the mossy fiber projection pattern.…”

Section: Developmental Origin Of the Dual Representation Of The Somatmentioning

confidence: 99%

Common Origin of the Cerebellar Dual Somatotopic Areas Revealed by Tracking Embryonic Purkinje Cell Clusters with Birthdate Tagging

Tran-Anh

Zhang

Nguyen-Minh

et al. 2020

eNeuro

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One of the notable characteristics of the functional localization in the cerebellar cortex is the dual representation of the body (somatotopy) along with its anterior-posterior axis. This somatotopy is conspicuous in the C1/C3 module, which is demarcated as the multiple zebrin-negative and weekly-positive stripes in dual paravermal areas in anterior and posterior lobules within the cerebellar compartments. In this report, we describe the early formation process of the cerebellar compartmentalization, particularly in the C1/C3 module. As developing PCs guide formation of the module-specific proper neuronal circuits in the cerebellum, we hypothesized that the rearrangement of embryonic Purkinje cell (PC) clusters shapes the adult cerebellar compartmentalization. By identifying PC clusters with immunostaining of marker molecules and genetical birthdate-tagging with Neurog2-CreER (G2A) mice, we clarified the three-dimensional spatial organization of the PC clusters and tracked the lineage relationships among the PC clusters from embryonic day 14.5 (E14.5) till E17.5. The number of recognized clusters increased from 9 at E14.5 to 37 at E17.5. Among E14.5 PC clusters, the c-l (central-lateral) cluster which lacked E10.5-born PCs divided into five c-l lineage clusters. They separately migrated underneath other clusters and positioned far apart mediolaterally as well as rostrocaudally by E17.5. They were eventually transformed mainly into multiple separate zebrin-negative and weakly-positive stripes, which together configured the adult C1/C3 module, in the anterior and posterior paravermal lobules. The results indicate that the spatial rearrangement of embryonic PC clusters is involved in forming the dual somatotopic areas in the adult mouse paravermal cerebellar cortex. Significance statement Genetically programmed morphogenetic processes in the embryonic brain can form a highly organized anatomical complex in the postnatal brain. The adult cerebellum has a complex functional localization; one of the challenging aspects of which is the dual representation of somatosensorimotor function in both the anterior and posterior paravermal areas. To elucidate morphogenetic processes of the intricate organization of the cerebellar cortex, we tracked lineages of early cerebellar PC clusters by birthdate-tagging methods. Starting with nine clusters at embryonic day 14.5, we clarified the differentiation of lineage of all clusters in later stages. Our results indicate that the spatial differentiation of embryonic PC clusters is involved in forming the basic cerebellar organization of the mouse brain.

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Dense projection of Stilling’s nucleus spinocerebellar axons that convey tail proprioception to the midline area in lobule VIII of the mouse cerebellum

Cited by 16 publications

References 46 publications

Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis

Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis

Single axonal morphology reveals high heterogeneity in spinocerebellar axons originating from the lumbar spinal cord in the mouse

Common Origin of the Cerebellar Dual Somatotopic Areas Revealed by Tracking Embryonic Purkinje Cell Clusters with Birthdate Tagging

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