Topographic mapping of motor pools onto skeletal muscles

Laskowski, Michael B.; Sanes, J. R.

doi:10.1523/jneurosci.07-01-00252.1987

Cited by 125 publications

(111 citation statements)

References 28 publications

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“…This interpretation is at least philosophically similar to that of the segmental identity of intercostal muscles, forelimb muscles, and the diaphragm proposed by Sanes and his co-workers (e.g., Wigston and Sanes, 1985;Wigston, 1986;Laskowski and Sanes, 1987;DeSantis et al, 1992). Both during development and during reinnervation, muscle fibers in different regions within these muscles receive selective innervation from motoneurons in different segmental regions of the spinal cord.…”

Section: Compartmental Identity Of Adult Musclessupporting

confidence: 79%

Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle

Gatesy

English

1993

Developmental Dynamics

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In adult rats, each neuromuscular compartment of the lateral gastrocnemius muscle (LG) is exclusively innervated by a primary branch of the LG nerve. In neonates, however, a small percentage of LG cells receives inputs from more than one primary nerve branch; these inputs are known as cross-compartmental. Cross-compartmental inputs are normally lost from the medial compartment of LG (LGm) by the 8th postnatal day. To investigate the mechanisms involved in the elimination of cross-compartmental inputs, muscle fibers in the LGm compartment were denervated by cutting the LGm nerve branch in 1-4 day old rat pups and in adult rats. We then assessed the degree of cross-compartmental innervation within the "denervated" compartment using intracellular recordings from neonatal muscle fibers or immunohistochemical staining for nerve cell adhesion molecule (N-CAM) and neurofilament protein in adult muscles. Following LGm axotomy in neonates, cross-compartmental innervation is more extensive than in controls and is present as late as 20 days after birth. Thus, in the absence of "native" LGm axons, neonatal cross-compartmental inputs proliferate by axonal sprouting and the formation of new synapses on vacant LGm fibers. In contrast, axotomized adults do not form new cross-compartmental inputs over the same time period. The differential response of neonates and adults to muscle nerve branch denervation is evidence for the existence of some form of compartment-specific recognition. We propose that compartmental identity either arises or becomes relatively more potent during ontogeny and normally acts selectively to eliminate foreign axons and deter the formation of new cross-compartmental inputs. 0 1993 Wiley-Liss, Inc.

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Section: Compartmental Identity Of Adult Musclessupporting

confidence: 79%

Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle

Gatesy

English

1993

Developmental Dynamics

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“…This topographic innervation did not correspond to the spatial distribution of fast and slow muscle regions and therefore may represent another level of target specificity. Some mammalian muscles are also topographically innervated (Browne, 1950;Swett et al, 1970;English and Weeks, 1984;Weeks and English, 1985;Donahue and English, 1987;Laskowski and Sanes, 1987;BaliceGordon and Thompson, 1988;Laskowski and High, 1989), supporting a role for A-P cues in muscle innervation.…”

Section: Determinants Of Selective Fasciculation and Pathfindingmentioning

confidence: 93%

Selective Fasciculation and Divergent Pathfinding Decisions of Embryonic Chick Motor Axons Projecting to Fast and Slow Muscle Regions

1998

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Proper motor function requires the precise matching of motoneuron and muscle fiber properties. The lack of distinguishing markers for early motoneurons has made it difficult to determine whether this matching is established by selective innervation during development or later via motoneuron-muscle fiber interactions. To examine whether chick motoneurons selectively innervate regions of their target containing either fast or slow muscle fibers, we backlabeled neurons from each of these regions with lipophilic dyes. We found that motor axons projecting to fast and slow muscle regions sorted into separate but adjacent fascicles proximally in the limb, long before they reached the muscle. More distally, these fascicles made divergent pathfinding decisions to course directly to the appropriate muscle fiber region. In contrast, axons projecting to different areas of an all-fast muscle did not fasciculate separately and became more intermingled as they coursed through the limb. Selective fasciculation of fast-and slow-projecting motoneurons was similar both before and after motoneuron cell death, suggesting that motoneurons specifically recognized and fasciculated with axons growing to muscle regions containing the appropriate muscle fiber type. Taken together, these results strongly support the hypothesis that "fast" and "slow" motoneurons are molecularly distinct before target innervation and that they use these differences to selectively fasciculate, pathfind to, and branch within the correct muscle fiber region from the outset of neuromuscular development.

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“…For analysis, the hemidiaphragm was divided into three anatomical regions (ventral, medial, and dorsal; Fig. 6I ), as the rostrocaudal axis of the PhMN pool topographically maps onto the ventrodorsal axis of the diaphragm (Laskowski and Sanes, 1987). Ipsilateral hemidiaphragm from the AAV-Gfa2-eGFP group showed milder NMJ abnormalities (Fig.…”

Section: Intraspinal Glt1 Overexpression Worsened Phrenic Nerve Axonamentioning

confidence: 99%

Overexpression of the Astrocyte Glutamate Transporter GLT1 Exacerbates Phrenic Motor Neuron Degeneration, Diaphragm Compromise, and Forelimb Motor Dysfunction following Cervical Contusion Spinal Cord Injury

Nicaise

Sannie

et al. 2014

J. Neurosci.

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A major portion of spinal cord injury (SCI) cases affect midcervical levels, the location of the phrenic motor neuron (PhMN) pool that innervates the diaphragm. While initial trauma is uncontrollable, a valuable opportunity exists in the hours to days following SCI for preventing PhMN loss and consequent respiratory dysfunction that occurs during secondary degeneration. One of the primary causes of secondary injury is excitotoxic cell death due to dysregulation of extracellular glutamate homeostasis. GLT1, mainly expressed by astrocytes, is responsible for the vast majority of functional uptake of extracellular glutamate in the CNS, particularly in spinal cord. We found that, in bacterial artificial chromosome-GLT1-enhanced green fluorescent protein reporter mice following unilateral midcervical (C4) contusion SCI, numbers of GLT1-expressing astrocytes in ventral horn and total intraspinal GLT1 protein expression were reduced soon after injury and the decrease persisted for Ն6 weeks. We used intraspinal delivery of adeno-associated virus type 8 (AAV8)-Gfa2 vector to rat cervical spinal cord ventral horn for targeting focal astrocyte GLT1 overexpression in areas of PhMN loss. Intraspinal delivery of AAV8-Gfa2-GLT1 resulted in transduction primarily of GFAP ϩ astrocytes that persisted for Ն6 weeks postinjury, as well as increased intraspinal GLT1 protein expression. Surprisingly, we found that astrocyte-targeted GLT1 overexpression increased lesion size, PhMN loss, phrenic nerve axonal degeneration, and diaphragm neuromuscular junction denervation, and resulted in reduced functional diaphragm innervation as assessed by phrenic nerve-diaphragm compound muscle action potential recordings. These results demonstrate that GLT1 overexpression via intraspinal AAV-Gfa2-GLT1 delivery exacerbates neuronal damage and increases respiratory impairment following cervical SCI.

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Topographic mapping of motor pools onto skeletal muscles

Cited by 125 publications

References 28 publications

Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle

Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle

Selective Fasciculation and Divergent Pathfinding Decisions of Embryonic Chick Motor Axons Projecting to Fast and Slow Muscle Regions

Overexpression of the Astrocyte Glutamate Transporter GLT1 Exacerbates Phrenic Motor Neuron Degeneration, Diaphragm Compromise, and Forelimb Motor Dysfunction following Cervical Contusion Spinal Cord Injury

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