Mechanisms of Activity-Dependent Motoneuron Development and Survival in the Chick Embryo
Neurons in the central and peripheral neurons system become capable of generating axon potentials, neurotransmitter release and synaptic transmission prior to their complete differentiation and in some cases this functional activity begins at remarkably early stages of embryogenesis (Provine, 1973; O’Donovan, 1999; Milner and Landmesser, 1999). Overtly this neuronal function is manifested as embryonic and fetal movements and reflexes that have been the focus of considerable research over the past century (Hamburger, 1963; Oppenheim, 1982; Gotttlieb, 1973; Michel and Moore, 1995). The developmentally early appearance of neuronal activity and behavior raises the obvious question of what adaptive role, if any, is served by prenatal neurobehavioral function. Early neural activity may be an epiphenomenon, in that it merely indicates that neuronal differentiation is proceeding normally. Alternatively, this early function may be a necessary feature of early nervous system organization acting to prepare the nervous system for its later role in mediating complex behavioral patterns (Crair, 1999). Finally, early neurobehavioral function may serve some immediate developmental function, a role I have previously called ontogenetic adaptations (Oppenheim, 1981; Hall and Oppenheim, 1986). For example, neuromuscular function and embryonic movements are known to play a role in the normal differentiation of skeletal muscles, synovial joints, lung differentiation and synapse formation between motorneurons and muscle. In the course of attempting to examine what role neuromuscular activity plays in the chick embryo, we discovered another apparent ontogenetic adaptation-like role for early neural function.
KeywordsChick Embryo Synapse Formation Motoneuron Survival Muscle Extract Developmental Psychobiology
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Calderó J, Prevette D, Mei X, Oakley RA, Li L, Milligan C, Houenou L, Burek M and Oppenheim RW (1998). Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J. Neurosci. 18:356–370.PubMedGoogle Scholar
Caroni P and Grandes P (1990). Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110:1307–1317.PubMedCrossRefGoogle Scholar
Caroni P and Becker M (1992). The down-regulation of growth associated proteins in motoneurons at the onset of synapse elimination is controlled by muscle activity and IGF-1. J. Neurosci. 12:3849–3861.PubMedGoogle Scholar
Caroni P Schneider C (1994). Signaling by insulin-like growth factors in paralyzed skeletal muscle: rapid induction of IGF-1 expression in muscle fibers and prevention of interstitial cell proliferation by IGF-BP5 and IGF-BP4. J. Neurosci. 14:3378–3388.PubMedGoogle Scholar
Caroni P, Schneider C, Kiefer MC and Zapf J (1994). Role of muscle insulin-like growth factors in nerve sprouting: suppression of terminal sprouting in paralyzed muscle by IGF-binding protein-5. J. Cell. Biol. 125:893–902.PubMedCrossRefGoogle Scholar
Crair MC (1999). Neuronal activity during development: permissive or restrictive? Curr. Opinion Neurobiol.
D’Costa AP, Prevette D, Houenou LJ, Wang S, Zackenfels K, Rohrer H, Zapf J, Caroni P and Oppenheim RW (1998). Mechanisms of insulin-like growth factor regulation of programmed cell death of developing avian motoneurons. J. Neurobiol. 36:379–394.PubMedCrossRefGoogle Scholar
Dahm L and Landmesser L (1988). The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130:621–644.PubMedCrossRefGoogle Scholar
Dahm L and Landmesser L (1991). The regulation of synaptogenesis during normal development and following activity blockade. J. Neurosci. 11:238–255.PubMedGoogle Scholar
Funakoshi H, Belluardo N, Arenas E, Yamamoto Y, Casabona A, Person H and Ibanez CF (1995). Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science. 268:1495–1499.PubMedCrossRefGoogle Scholar
Glucksmann A (1951). Cell death in normal vertebrate ontogeny. Biol. Rev. 26:59–86.CrossRefGoogle Scholar
Goodman CS and Shatz CJ (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell
Gottlieb G, ed (1973). Studies in the Development of Behavior and the Nervous System: Behavioral Embryology. Academic, New York.Google Scholar
Hall WG and Oppenheim RW (1986). Developmental psychobiology: Prenatal, perinatal and early postnatal aspects of behavioral development. Ann. Rev. Psychol. 38:91–128.CrossRefGoogle Scholar
Hamburger V (1963). Some aspects of the embryology of behavior. Quart. Rev. Biol. 38:342–365.PubMedCrossRefGoogle Scholar
Hamburger V (1975). Cell death in the development of the lateral motor column of the chick embryo. J. Comp. Neurol. 160:535–546.PubMedCrossRefGoogle Scholar
Hamburger V and Oppenheim RW (1982). Naturally occurring neuronal death in vertebrates. Neurosci. Comment. 1:38–55.Google Scholar
Hory-Lee F and Frank F (1995). The nicotinic blocking agents d-tubocurare and α-bungarotoxin save motoneurons from naturally occurring death in the absence of neuromuscular blockade. J. Neurosci. 26:6453–6460.Google Scholar
Houenou LJ, McManaman JL, Prevette D and Oppenheim RW (1991). Regulation of putative muscle-derived neurotrophic factors by muscle activity and innervation: in vivo and in vitro studies. J. Neurosci. 11:2829–2837.PubMedGoogle Scholar
Ishii DN (1989). Relationship of insulin-like growth factor II gene expression in muscle to synaptogenesis. Proc. Natl. Acad. Sci. 86:2898–2902.PubMedCrossRefGoogle Scholar
Kiefer MD, Schmid C, Waldvogel M, Schlaepfer I, Futo E, Masiaiz FR, Green K, Barr PJ and Zapf J (1992). Characterization of recombinant human insulin-like growth factor binding protein-4, 5 and 6 produced in yeast. J. Biol. Chem. 267:12692–12699.PubMedGoogle Scholar
Landmesser L and Szente M (1987). Activation patterns of embryonic chick hindlimb muscles following blockade of activity and motoneuron cell death. J. Physiol. 380:157–174.Google Scholar
Landmesser L (1992). The relationship of intramuscular nerve branching and synaptogenesis to motoneuron survival. J. Neurobiol. 23:1131–1139.PubMedCrossRefGoogle Scholar
Michel GE and Moore CL (1995). Developmental Psychobiology. MIT Press, Cambridge, MA.Google Scholar
Milner LD and Landmesser LT (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J. Neurosci.
Neff TN, Prevette D, Houenou LJ, Lewis ME, Glicksman MA, Yin Q-W and Oppenheim RW (1993). Insulin-like growth factors: Putative muscle-derived trophic agents that promote motoneuron survival. J. Neurobiol. 24:1578–1588.PubMedCrossRefGoogle Scholar
Nguyen QT, Parsadanian A, Snider WD and Lichtman JW (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science
O’Donovan MJ (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr. Opinion Neurobiol.
Oppenheim RW (1981). Ontogenetic adaptations and retrogressive processes in the development of the nervous system and behavior. In Connolly, K and Prechtl, H, eds. Maturation and Development: Biological and Psychological Perspectives. pp. 198–215. Lippincott, Philadelphia.Google Scholar
Oppenheim RW (1982). The neuroembryological study of behavior: Progress, problems, perspectives. Curr. Topics Dev. Biol. 17:257–309.CrossRefGoogle Scholar
Oppenheim RW and Chu-Wang IW (1983). Aspects of naturally occurring motoneuron death in the chick spinal cord during embryonic development. In Burnstock, G and Vrbova, G (Eds): Somatic and Autonomic Nerve-Muscle Interactions. Amsterdam: Elsevier, pp. 57–107.Google Scholar
Oppenheim RW and Haverkamp L (1986). Early development of behavior and the nervous system: An embryological perspective. In Blass, EM, ed. Handbook of Behavioral Neurobiology, vol. 8, Developmental Psychobiology and Developmental Neurobiology pp. 35–97. Plenum, New York.Google Scholar
Oppenheim RW, Houenou L, Pincon-Raymond M, Powell JA, Rieger F and Standish LJ (1986). The development of motoneurons in the embryonic spinal cord of the mouse mutant, muscular dysgenesis (mdg/mdg
): survival, morphology and biochemical differentiation. Dev. Biol.
Oppenheim RW (1989). The neurotrophic theory and naturally occurring motoneuron death. Trends Neurosci. 12:252–255.PubMedCrossRefGoogle Scholar
Oppenheim RW (1996). Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron. 17:195–197.PubMedCrossRefGoogle Scholar
Oppenheim RW, Prevette D and Wang SW (1996). The rescue of avian motoneurons by activity blockade at the neuromuscular junction. Soc. Neurosci. Abstr. 22:44.Google Scholar
Oppenheim RW, Prevette D, Houenou LJ, Pincon-Raymond M, Dimitriadou V, Donevan A, O’Donovan M, Wenner P, McKemy D and Allen PD (1997). Neuromuscular development in the avian paralytic mutant crooked neck dwarf (cn/cn): Further evidence for the role of neuromuscular activity in motoneuron survival. J. Comp. Neurol. 381:353–372.PubMedCrossRefGoogle Scholar
Oppenheim RW (1999). Programmed cell death. In Zigmond, MJ et al.
, eds. Fundamental Neuroscience pp. 581–609. Academic, New York.Google Scholar
Pittman R and Oppenheim RW (1978). Neuromuscular blockade increases motoneuron survival during normal cell death in the chick embryo. Nature 271:364–366.PubMedCrossRefGoogle Scholar
Pittman R and Oppenheim RW (1979). Evidence that a functional neuromuscular interaction is involved in the regulation of naturally occurring cell death and the stabilization of synapses. J. Comp. Neurol. 187:425–446.PubMedCrossRefGoogle Scholar
Provine RR (1973). Neurophysiological aspects of behavior development in the chick embryo. In Gottlieb, G, ed. Studies on the Development of Behavior and the Nervous System: Behavioral Embryology pp. 77–102. Academic, New York.Google Scholar
Purves D (1988). Body and Brain, A Trophic Theory of Neuronal Connections. Harvard, Cambridge, MA.Google Scholar
Raff MC (1992). Social controls on cell survival and cell death. Nature 356:397–400.PubMedCrossRefGoogle Scholar
Renshaw GMC and Goldie R (1996). Neuronal bungarotoxin displaces [125
I]α-bungarotoxin binding at the neuromuscular junctions as well as to the spinal cord during embryogenesis. Brain Res.
Role LW and Berg DK (1996). Nicotinic receptors in the development and modulation of CNS synapses. Neuron. 16:1077–1085.PubMedCrossRefGoogle Scholar
Snider WD (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell. 77:627–638.PubMedCrossRefGoogle Scholar
Son YJ, Trachtenberg JT and Thompson WJ (1996). Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci. 19:280–285.PubMedCrossRefGoogle Scholar
Tanaka H (1987). Chronic application of curare does not increase the level of motoneuron-promoting survival activity in limb muscle extracts during the naturally occurring motoneuron death period. Dev. Biol. 124:347–357.PubMedCrossRefGoogle Scholar
Tang J and Landmesser L (1993). Reduction of intramuscular nerve branching and synaptogenesis is correlated with decreases in motoneuron survival. J. Neurosci. 13:3095–3103.PubMedGoogle Scholar
Vijayaraghavan S, Pugh PC, Zhaug ZW, Rathouz MM and Berg DK (1992). Nicotinic receptors that bind α-bungarotoxin on neurons raise intracellular free Ca2+
. Neuron. 8:353–362.PubMedCrossRefGoogle Scholar
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