The Ancient Origins of Neural Substrates for Land Walking

Jung, Hye Ra; Baek, Min Won; D’Elia, Kristen P.; Boisvert, Catherine A.; Currie, Peter D.; Tay, Boon Hui; Venkatesh, Byrappa; Brown, Stuart M.; Heguy, Adriana; Schoppik, David; Dasen, Jeremy S.

doi:10.1016/j.cell.2018.01.013

Cited by 76 publications

(105 citation statements)

References 56 publications

(87 reference statements)

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“…A previous study reported that the localization of LMC neurons expands posteriorly in the neural tube of skates (24). However, the peripheral innervation pattern of batoid spinal nerves during embryogenesis has not been studied in detail.…”

Section: Branching Of Spinal Nerves Into the Body Wall And Pectoral Finsmentioning

confidence: 96%

“…Loss of the HoxC cluster results in high FoxP1 expression, and the through development of the LMC between brachial and lumbar domains in skates (24). Unexpectedly, a previous study identified a minor population of MNs that is similar to the HMC at pectoral and pelvic domains with LMC in the neural tube of skates (24), implying that skates retain unique patterns of innervation at the brachial level compared with other finned vertebrates. However, developmental patterns of peripheral nerves in skates and other rays have not yet been sufficiently investigated.…”

Section: Introductionmentioning

confidence: 92%

“…Previous studies have revealed evolutionary diversity of MNs for paired appendages of elephant sharks, skates, and zebrafish (24,26). However, the molecular mechanisms that coordinate evolution of appendage muscles, nerves, and skeletons remains unknown.…”

Section: Dynamic Rearrangements Of Hox Expression Patterns In Skatesmentioning

confidence: 99%

“…Intriguingly, skates (Leucoraja erinacea) and catsharks (Scyliorhinus canicular) lost the HoxC cluster during evolution (22,23). Loss of the HoxC cluster results in high FoxP1 expression, and the through development of the LMC between brachial and lumbar domains in skates (24). Unexpectedly, a previous study identified a minor population of MNs that is similar to the HMC at pectoral and pelvic domains with LMC in the neural tube of skates (24), implying that skates retain unique patterns of innervation at the brachial level compared with other finned vertebrates.…”

Section: Introductionmentioning

confidence: 99%

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The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

Turner

Mikalauskaite

Barone

et al. 2019

Preprint

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Appendage patterning and evolution have been active areas of inquiry for the past two centuries. While most work has centered on the skeleton, particularly that of amniotes, the evolutionary origins and molecular underpinnings of the neuromuscular diversity of fish appendages have remained enigmatic. The fundamental pattern of segmentation in amniotes, for example, is that all muscle precursors and spinal nerves enter either the paired appendages or body wall at the same spinal level. The condition in finned vertebrates is not understood. To address this gap in knowledge, we investigated the development of muscles and nerves in unpaired and paired fins of skates and compared them to those of chain catsharks. During skate and shark embryogenesis, cell populations of muscle precursors and associated spinal nerves at the same axial level contribute to both appendages and body wall, perhaps representing an ancestral condition of gnathostome appendicular neuromuscular systems. Remarkably in skates, this neuromuscular bifurcation as well as colinear Hox expression extend posteriorly to pattern a broad paired fin domain. In addition, we identified migratory muscle precursors (MMPs), which are known to develop into paired appendage muscles with Pax3 and Lbx1 gene expression, in the dorsal fins of skates. Our results suggest that muscles of paired fins have evolved via redeployment of the genetic program of MMPs that were already involved in dorsal fin development. Appendicular neuromuscular systems most likely have emerged as side branches of body wall neuromusculature and have been modified to adapt to distinct aquatic and terrestrial habitats.

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Section: Branching Of Spinal Nerves Into the Body Wall And Pectoral Finsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 92%

Section: Dynamic Rearrangements Of Hox Expression Patterns In Skatesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

Turner

Mikalauskaite

Barone

et al. 2019

Preprint

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“…In situ hybridization of tissue sections was performed as previously described using DIG labeled probes 48 .…”

Section: In Situ Hybridizationmentioning

confidence: 99%

Molecular Logic of Spinocerebellar Tract Neuron Diversity and Connectivity

Baek

Menon

Jessell

et al. 2019

Preprint

Self Cite

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Coordinated motor behaviors depend on feedback communication between peripheral sensory systems and central circuits in the brain and spinal cord. Relay of muscle and tendonderived sensory information to the CNS is facilitated by functionally and anatomically diverse groups of spinocerebellar tract neurons (SCTNs), but the molecular logic by which SCTN diversity and connectivity is achieved is poorly understood. We used single cell RNA sequencing and genetic manipulations to define the mechanisms governing the molecular profile and organization of SCTN subtypes. We found that SCTNs relaying proprioceptive sensory information from limb and axial muscles are generated through segmentally-restricted actions of specific Hox genes. Loss of Hox function disrupts SCTN subtype-specific transcriptional programs, leading to defects in the connections between proprioceptive sensory neurons, SCTNs, and the cerebellum. These results indicate that Hox-dependent genetic programs play essential roles in the assembly of the neural circuits required for proprioception.

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Development of fin‐innervating motor neurons after peripheral target removal in medaka fish

Chiba

Soma

Watanabe

et al. 2020

Developmental Neurobiology

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Peripheral targets regulate the development and survival of the nerve centers that serve them, because the elimination of the target normally results in massive death of the developing neurons that innervate it. This widely accepted theory appears to be well supported by developing limbs and their innervation in tetrapods, but it is unclear whether this concept applies to primitive vertebrates that have paired appendages. In this study, we examined the development of spinal motor neurons following pectoral fin bud removal (FBR) in medaka fish. After FBR, motor axons initially extended to the plexus region in a morphologically normal pattern. During the period of fin innervation, motor axons in the FBR‐medaka failed to form the normal brachial plexus and elongated ventrally toward the abdominal region. In the ventral horn that would normally innervate the pectoral fin, however, neurons did not undergo cell death following FBR. There were no differences in the numbers of axons in the ventral roots between the FBR and control sides. Motor neuron markers, RALDH2 and FOXP1, that are expressed in limb‐innervating motor neurons in the lateral motor column in tetrapods, were also expressed in the ventral horns of both the control and FBR sides in medaka fish. These results suggest that, although both tetrapod and medaka motor neurons share the same molecular characteristics for innervating paired appendages, the fates of neurons differ following the removal of their peripheral target. Therefore, the relationship between the peripheral target and its nerve center may be altered among vertebrates.

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The Ancient Origins of Neural Substrates for Land Walking

Cited by 76 publications

References 56 publications

The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

Molecular Logic of Spinocerebellar Tract Neuron Diversity and Connectivity

Development of fin‐innervating motor neurons after peripheral target removal in medaka fish

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