The formation of appropriate central and peripheral connexions by foreign sensory neurones of the bullfrog

Frank, Eric; Westerfield, Monte

doi:10.1113/jphysiol.1982.sp014126

Cited by 56 publications

(28 citation statements)

References 14 publications

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“…For example, if thoracic DRG, which normally lack any muscle spindle afferents, are forced to supply forelimb muscles, these ganglia will produce muscle spindle afferents that project to the appropriate forelimb motoneurons (Frank and Westerfield, 1982;Smith and Frank, 1987). These results indicate that some signal(s) from peripheral targets can determine both the general identity of sensory neurons (i.e., the muscle spindle afferent phenotype) and their specific identity in terms of which motoneurons they choose as synaptic partners.…”

Section: Abstract: Neurotrophins; Sensory Neurons; Muscle Spindle Afmentioning

confidence: 78%

“…These studies showed that limb muscle could promote the development of muscle spindle afferents in thoracic DRG, which do not normally produce neurons of this phenotype. Moreover, these neurons made connections with motoneurons that were appropriate for the specific muscle that was supplied (Frank and Westerfield, 1982;Smith and Frank, 1987). Thus, signals from limb muscle can determine both the general phenotype of sensory neurons (i.e., muscle spindle afferent) and which motoneurons they will choose as synaptic partners.…”

Section: Nt3 and The Specification Of Muscle Spindle Afferentsmentioning

confidence: 99%

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Neurotrophin-3 Promotes the Differentiation of Muscle Spindle Afferents in the Absence of Peripheral Targets

et al. 1997

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The neurons of the dorsal root ganglia (DRG) that supply muscle spindles require target-derived factors for survival. One necessary factor for these neurons is neurotrophin-3 (NT3). To determine whether NT3 can promote the survival of these neurons in the absence of other target-derived factors, we analyzed the effects of exogenous NT3 after early limb bud deletion in the chick. In control embryos, limb bud deletion eliminated ϳ90% of the trkC-positive (trkCϩ) neurons in lumbar DRG on the deleted side. In addition, the deletion led to a dramatic loss of collateral sensory projections to motoneurons. Exogenous NT3 restored a normal population of trkCϩ neurons in lumbar DRG on the deleted side and increased the number of trkCϩ neurons in DRG with normal targets (contralateral lumbar and thoracic). The effect was highly selective; NT3 increased the number of trkCϩ neurons without significantly changing the number of either trkAϩ or trkBϩ neurons. The effect of NT3 was attributable to the rescue of DRG neurons from cell death, because exogenous NT3 reduced the number of pyknotic nuclei without significantly altering proliferation. Analysis of spinal projections showed further that many of the trkCϩ neurons rescued by NT3 projected to the ventral spinal cord. These neurons thus had central projections characteristic of muscle spindle afferents. Together, our results indicate that NT3 signaling is both necessary and sufficient for the development of the proprioceptive phenotype, even in the absence of other signals from limb muscle. Key words: neurotrophins; sensory neurons; muscle spindle afferents; survival; specification; differentiation; development; spinal cord projections; muscleThe dorsal root ganglia (DRG) are composed of several functionally diverse populations of sensory neurons that form distinct patterns of central connections within the spinal cord. For example, most DRG neurons are small-diameter cutaneous afferents (nociceptors and thermoceptors) that project to the superficial layers of the dorsal horn. In contrast, the comparatively small population of large-diameter DRG neurons that supply muscle spindles project to the ventral horn and make monosynaptic connections with motoneurons (for review, see Willis and Coggeshall, 1991; also see Ruit et al., 1992). Thus, different populations of sensory neurons have distinct identities that can be defined on the basis of their central and peripheral projections.Developmental studies in the frog have shown that the identity of sensory neurons is dependent on their peripheral targets, in that the peripheral target can determine the pattern of central connections. For example, if thoracic DRG, which normally lack any muscle spindle afferents, are forced to supply forelimb muscles, these ganglia will produce muscle spindle afferents that project to the appropriate forelimb motoneurons (Frank and Westerfield, 1982;Smith and Frank, 1987). These results indicate that some signal(s) from peripheral targets can determine both the general identity of sensory neurons (i...

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Section: Abstract: Neurotrophins; Sensory Neurons; Muscle Spindle Afmentioning

confidence: 78%

Section: Nt3 and The Specification Of Muscle Spindle Afferentsmentioning

confidence: 99%

Neurotrophin-3 Promotes the Differentiation of Muscle Spindle Afferents in the Absence of Peripheral Targets

et al. 1997

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“…When embryonic amphibian sensory afferents were redirected, their central projections were appropriate for the new target (Frank and Westerfield, 1982;Frank, 1987, 1988). Rerouting of sensory afferents from muscle to skin alters Figure 6.…”

Section: Discussionmentioning

confidence: 99%

The Generation of Neuronal Heterogeneity in a Rat Sensory Ganglion

Hall

Hickman

et al. 1997

J. Neurosci.

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Adult sensory neurons differ chemically, morphologically, and functionally, but the factors that generate their diversity remain unclear. For example, neuropeptides are generally found in small neurons, whereas abundant neurofilament is common in large neurons. Neurons containing the neuropeptides calcitonin gene-related peptide (CGRP) or substance P were quantified using immunohistochemistry in rat lumbar dorsal root ganglion (DRG) at times before and after sensory neurons contact central and peripheral targets in vivo. No neurons in the newly formed DRG expressed neuropeptide or neuropeptide mRNA, but neuropeptides were detectable about the time that axons connect with peripheral targets. To determine the requirement for target in neuropeptide regulation, embryonic DRG neurons were isolated at times before central and peripheral connections had formed, placed in culture, and immunocytochemically assayed for CGRP and substance P. Cultured neurons expressed neuropeptides with a time course and in proportions similar to those in vivo. Thus, some neurons in the embryonic DRG seem to be intrinsically specified to later express CGRP and substance P. The percentage of CGRP-immunoreactive neurons was not changed by cell density, non-neuronal cells, neurotrophins in addition to nerve growth factor (NGF), or antibody inactivation of neurotrophin-3 in the presence of NGF. To test the role of extrinsic cues on CGRP expression, DRG neurons were co-cultured with potential target tissues. Coculture with a rat epidermal or smooth muscle cell line increased the proportion of CGRP-containing neurons, whereas primary skeletal muscle and 3T3 cells had no effects. Thus, multiple appropriate sensory neuron phenotypes arise in a regulated fashion in cultured neurons isolated before target connections have formed, and some candidate target tissues can modulate that intrinsic expression pattern. Key words: neuropeptides; substance P; calcitonin generelated peptide; neurofilament; nociceptive; sensory ganglion; target tissue; skin; neurotrophinA striking feature of the adult vertebrate sensory nervous system is the diversity of neuronal cell types that perform together to maintain homeostasis and convey information about the environment. During development, specific neurons must be generated in appropriate locations and connect discretely to both peripheral targets and the CNS for functional integrity. Thus, it is important to understand not only how the phenotype is generated but also how neurons match targets. This study examines the developmental regulation of sensory neurons containing calcitonin generelated peptide (CGRP) that predominantly contact visceral and cutaneous peripheral target end organs in vivo.Adult rat sensory neurons can express neuromodulatory neuropeptides, but the factors that regulate their initial expression remain unknown. Cutaneous afferents appear in rat proximal hindlimb on embryonic days 14 -15 (E14 -E15) and in skin of distal toes at E16 -E17 (Reynolds et al

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“…Furthermore, minor changes in the central connections of the adult mammalian central nervous system have been observed to result from changes in motoneurone innervation (Eccles, Eccles & Magni, 1960;Eccles, Eccles, Shealy & Willis, 1962;Mendell & Scott, 1975;Tsukahara & Fujita, 1976). Frank & Westerfield (1982) have suggested that bull-frog sensory ganglion neurones forced to project to regionally inappropriate targets may be respecified to make functionally appropriate monosynaptic connections with motoneurones that they would normally not innervate (see also Hollyday & Mendell, 1975). In the chick embryo, spinal ganglia neurones do not innervate limb regions or motoneurones left uninnervated by removal of neural crest cells (Eide, Jansen & Ribchester, 1982) or small segments of the neural tube (Honig, 1979).…”

Section: Discussionmentioning

confidence: 99%

Activation patterns of embryonic chick lumbosacral motoneurones following large spinal cord reversals.

Vogel

1987

The Journal of Physiology

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SUMMARY1. Embryonic chick motoneurones were caused to innervate inappropriate hindlimb muscles by rotating the presumptive lumbosacral region of the neural tube in stage 15-16 embryos which is prior to the outgrowth of motoneurone axons.2. The activation patterns of motoneurones in control and spinal cord reversal embryos were analysed from electromyographic (e.m.g.) recordings of stage 36 limb muscles during evoked movement sequences in an isolated spinal cord-limb preparation. Histograms representing the frequency of activation were constructed for each muscle. The muscle's pattern of activation was classified as flexor-like or extensor-like and compared to the activation patterns of control muscles.3. A series of control operations was performed in which the prospective lumbosacral region of the neural tube was removed and replaced in its original orientation. Muscles in these embryos were innervated by their normal motoneurone pools and they were activated normally, indicating that the neural tube operation per se does not alter the activation pattern of motoneurones. Furthermore, some muscles (twelve out of sixty-one) in spinal cord reversal embryos had normal activation patterns and appeared to be innervated by their original motoneurones. Based on these results and the result of a previous study (Landmesser & O 'Donovan, 1984 b), it is concluded that motoneurones in reversed spinal cords are activated in a manner appropriate for their original identity.4. The majority of muscles (thirty-three out of sixty-one) in large spinal cord reversal embryos were activated during an appropriate phase of the kicking cycle.Of the remaining muscles, 16 % were activated inappropriately (i.e. extensor muscles were activated as flexors, and vice versa), and 30 % had a novel 'mixed' flexor-and extensor-like activation pattern. However, the activation pattern of most muscles differed markedly from that of any other control muscles regardless of whether the muscle was activated appropriately or inappropriately as a flexor or extensor. The abnormal activation patterns are a likely consequence of the diffuse distribution of inappropriate motoneurones projecting to foreign muscles in embryos with large spinal cord reversals. Since it is likely that motoneurones are still activated according * Present address:

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The formation of appropriate central and peripheral connexions by foreign sensory neurones of the bullfrog

Cited by 56 publications

References 14 publications

Neurotrophin-3 Promotes the Differentiation of Muscle Spindle Afferents in the Absence of Peripheral Targets

Neurotrophin-3 Promotes the Differentiation of Muscle Spindle Afferents in the Absence of Peripheral Targets

The Generation of Neuronal Heterogeneity in a Rat Sensory Ganglion

Activation patterns of embryonic chick lumbosacral motoneurones following large spinal cord reversals.

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