Stabilization of Axon Branch Dynamics by Synaptic Maturation

Ruthazer, Edward S.; Li, Jianli; Cline, Hollis T.

doi:10.1523/jneurosci.0069-06.2006

Cited by 178 publications

(219 citation statements)

References 48 publications

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“…Numerous studies have revealed developmentally regulated synaptic maturation during periods when the expression of LTP is also robust (Crair and Malenka, 1995;Rumpel et al, 1998;Chen and Regehr, 2000), and this synaptic maturation is correlated with axon remodeling during map refinement (Meyer and Smith, 2006;Ruthazer et al, 2006). Whether the experimentally induced LTP is physiologically relevant to circuit formation is unclear, however, because of the wide variety of induction protocols used and the lack of information about natural activity patterns during development.…”

Section: Resultsmentioning

confidence: 99%

“…Interestingly, chronic NMDAR blockade serves to increase RGC arbor branch dynamics, suggesting that NMDAR activity and synaptic maturation normally stabilizes retinotectal projections during circuit formation (Rajan et al, 1999). Recent in vivo imaging of zebrafish and tadpole retinotectal axons reveals that synapse formation and maturation are tightly correlated with branch dynamics and may play an instructive role in arbor remodeling during map formation (Meyer and Smith, 2006;Ruthazer et al, 2006). Indeed, correlated activity is known to regulate RGC axon branch dynamics during development (Ruthazer et al, 2003;Hua et al, 2005), offering additional evidence that the refinement of retinotopic projections proceeds through activitydependent instruction and synaptic competition.…”

Section: Model Of Synaptic-competition-based Retinotopic Map Refinementmentioning

confidence: 99%

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Retinocollicular Synapse Maturation and Plasticity Are Regulated by Correlated Retinal Waves

Shah¹,

Crair²

2008

J. Neurosci.

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During development, spontaneous retinal waves are thought to provide an instructive signal for retinotopic map formation in the superior colliculus. In mice lacking the ␤2 subunit of nicotinic ACh receptors (␤2 Ϫ/Ϫ ), correlated retinal waves are absent during the first postnatal week, but return during the second postnatal week. In control retinocollicular synapses, in vitro analysis reveals that AMPA/ NMDA ratios and AMPA quantal amplitudes increase during the first postnatal week while the prevalence of silent synapses decreases. In age-matched ␤2 Ϫ/Ϫ mice, however, these parameters remain unchanged through the first postnatal week in the absence of retinal waves, but quickly mature to control levels by the end of the second week, suggesting that the delayed onset of correlated waves is able to drive synapse maturation. To examine whether such a mechanistic relationship exists, we applied a "burst-based" plasticity protocol that mimics coincident activity during retinal waves. We find that this pattern of activation is indeed capable of inducing synaptic strengthening [long-term potentiation (LTP)] on average across genotypes early in the first postnatal week [postnatal day 3 (P3) to P4] and, interestingly, that the capacity for LTP at the end of the first week (P6 -P7) is significantly greater in immature ␤2 Ϫ/Ϫ synapses than in mature control synapses. Together, our results suggest that retinal waves drive retinocollicular synapse maturation through a learning rule that is physiologically relevant to natural wave statistics and that these synaptic changes may serve an instructive role during retinotopic map refinement.

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Section: Resultsmentioning

confidence: 99%

Section: Model Of Synaptic-competition-based Retinotopic Map Refinementmentioning

confidence: 99%

Retinocollicular Synapse Maturation and Plasticity Are Regulated by Correlated Retinal Waves

Shah¹,

Crair²

2008

J. Neurosci.

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“…Images were collected from anesthetized tadpoles (0.02% MS-222; Sigma) positioned under a glass coverslip in a Sylgard chamber. Animal preparation, laser sources, signal amplification, PMT specifications, and YFP/CFP filter sets have been described previously (48). Using the raw image stacks (1-1.5-m z interval), manual reconstructions of the dendritic arbor in three dimensions were generated and then analyzed for total dendritic branch length, branch-tip number, and 3D Sholl analysis (29); radius interval 1 m, averaged over 10-m bins) using Object-Image macros (written by Dr. E. Ruthazer, McGill University, Quebec).…”

Section: Methodsmentioning

confidence: 99%

The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

Bestman

Cline

2008

Proc. Natl. Acad. Sci. U.S.A.

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Visual system development requires experience-dependent mechanisms that regulate neuronal structure and function, including dendritic arbor growth, synapse formation, and stabilization. Although RNA binding proteins have been shown to affect some forms of synaptic plasticity in adult animals, their role in the development of neuronal structure and functional circuitry is not clear. Using two-photon time-lapse in vivo imaging and electrophysiology combined with morpholino-mediated knockdown and expression of functional deletion mutants, we demonstrate that the mRNA binding protein, cytoplasmic polyadenylation element binding protein1 (CPEB1), affects experience-dependent neuronal development and circuit formation in the visual system of Xenopus laevis. These data indicate that sensory experience controls circuit development by regulating translational activity of mRNAs.circuit integration ͉ experience-dependent plasticity ͉ in vivo imaging ͉ visual system ͉ whole-cell recording D uring CNS development, neuronal structure, synaptic connections, and circuit functions change in response to sensory input. Although the regulation of mRNA translation and new protein synthesis have been implicated in some forms of neuronal plasticity in adult animals (1, 2), their role in experience-dependent sensory system plasticity has not been addressed (3). In the brain, the translation of many mRNAs is regulated by their association with ribonucleoprotein (RNP) granules, which are composed of core RNA binding proteins, translational machinery, and mRNAs (4). RNA binding proteins package specific mRNAs within RNP granules, regulate their transport into dendrites, and in principle, could temporally and spatially govern their translation in response to synaptic activity (4). Because of these features, mRNA binding proteins are in a unique position to control developmental events through the coordinated translation of a functionally related cohort of mRNAs (5, 6). Indeed, local protein synthesis affords neurons the ability to stabilize changes in synaptic connections and alter neuronal output (7). Recent studies indicate that cytoplasmic polyadenylation element binding protein 1 (CPEB1) is among a handful of RNA binding proteins that regulate dendritic protein synthesis and synaptic plasticity in vitro (8). Although studies in mutant mice implicate CPEB1 in some forms of synaptic and spine plasticity and in memory extinction (9-11), no studies have examined the potential role of CPEB1 in dendritic arbor development, experience-dependent structural plasticity, or the integration of neurons into a functional circuit in an intact animal.CPEB1 (Orb in D. melanogaster) is a member of an evolutionarily conserved family of RNA binding proteins that is expressed in the brain (in vertebrates, CPEB1-4). While all members are defined by the presence of RNA recognition motifs in their carboxy-terminals, CPEB1 is the only member that targets mRNAs containing cytoplasmic polyadenylation elements (CPEs) in their 3Ј untranslated regions (12). Origina...

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“…Studies in the retinotectal projection, for example, have shown that branching and synaptogenesis are closely connected and interdependent (Meyer and Smith, 2006;Ruthazer et al, 2006).…”

Section: Ephrina5/trk Interaction In Synaptic Plasticitymentioning

confidence: 99%

“…J. Huang et al, 1999;Alsina et al, 2001;Meyer and Smith, 2006;Ruthazer et al, 2006). Moreover, although there is ample evidence for a role of the EphB subfamily in axonal branching and synaptic plasticity, less is known about that of the EphA subfamily (P. P. W.…”

Section: Ephrina5/trk Interaction In Synaptic Plasticitymentioning

confidence: 99%

A TrkB/EphrinA Interaction Controls Retinal Axon Branching and Synaptogenesis

Marler¹,

Becker-Barroso²,

Martı́nez³

et al. 2008

J. Neurosci.

148

176

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Toward understanding topographically specific branching of retinal axons in their target area, we have studied the interaction between neurotrophin receptors and members of the Eph family. TrkB and its ligand BDNF are uniformly expressed in the retina and tectum, respectively, and exert a branch-promoting activity, whereas EphAs and ephrinAs are expressed in gradients in retina and tectum and can mediate a suppression of axonal branching. We have identified a novel cis interaction between ephrinA5 and TrkB on retinal ganglion cell axons. TrkB interacts with ephrinA5 via its second cysteine-rich domain (CC2), which is necessary and sufficient for binding to ephrinA5. Their functional interaction is twofold: ephrinA5 augments BDNF-promoted retinal axon branching in the absence of its activator EphA7-Fc, whereas EphA7-Fc application abolishes branching in a local and concentration-dependent manner. The importance of TrkB in this process is shown by the fact that overexpression of an isolated TrkB-CC2 domain interfering with the ephrinA/TrkB interaction abolishes this regulatory interplay, whereas knockdown of TrkB via RNA interference diminishes the ephrinA5-evoked increase in branching. The ephrinA/Trk interaction is neurotrophin induced and specifically augments the PI-3 kinase/Akt pathway generally known to be involved in the promotion of branching. In addition, ephrinAs/TrkB modulate axon branching and also synapse formation of hippocampal neurons. Our findings uncover molecular mechanisms of how spatially restricted axon branching can be achieved by linking globally expressed branch-promoting with differentially expressed branch-suppressing activities. In addition, our data suggest that growth factors and the EphA-ephrinA system interact in a way that affects axon branching and synapse development.

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Stabilization of Axon Branch Dynamics by Synaptic Maturation

Cited by 178 publications

References 48 publications

Retinocollicular Synapse Maturation and Plasticity Are Regulated by Correlated Retinal Waves

Retinocollicular Synapse Maturation and Plasticity Are Regulated by Correlated Retinal Waves

The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

A TrkB/EphrinA Interaction Controls Retinal Axon Branching and Synaptogenesis

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