Activity-Dependent Cortical Target Selection by Thalamic Axons

Catalano, Susan M.; Shatz, Carla J.

doi:10.1126/science.281.5376.559

Cited by 249 publications

(150 citation statements)

References 25 publications

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“…The subplate cells in the developing cortex, a transient cell layer above the subventricular zone and below the emerging cortical layers, serve as a temporary way-station where axons pause before entering the emerging permanent cortical layers (Luskin and Shatz 1985;Ghosh and Shatz 1992). The subplate is crucial for proper guidance and afferent invasion of the cortex (Catalano and Shatz 1998;Kanold et al 2003). The subplate is similar to the chiasmatic neurons described above, in that these cell groups disappear (or transit into other cell types) as the brain matures.…”

Section: Substrata In Vivomentioning

confidence: 88%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

130

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Axons follow highly stereotyped and reproducible trajectories to their targets. In this review we address the properties of the first pioneer neurons to grow in the developing nervous system and what has been learned over the past several decades about the extracellular and cell surface substrata on which axons grow. We then discuss the types of guidance cues and their receptors that influence axon extension, what determines where cues are expressed, and how axons respond to the cues they encounter in their environment.T his article provides an overview of how growth cones respond to the cellular substrata and molecular cues they encounter as they extend through the developing nervous system. It elaborates on the primer by Kolodkin and TessierLavigne (2010) and touches on many of the topics covered in greater detail in the articles that follow. The first sections describe how axons extend in a directed manner, the substrata on which they grow, interactions between pioneer and follower axons, and growth cone behaviors in emerging tracts and at decision points. The subsequent sections discuss examples of specific cues, their distributions, how their distributions are determined, and how growth cones integrate multiple cues during pathfinding. AXONS EXTEND IN VIVO IN A DIRECTED MANNERThe first person to visualize the growing tips of axons, Ramon y Cajal, recognized that axons for the most part grow very efficiently towards their ultimate targets. He was a strong advocate for axons finding their way in response to chemotactic cues:"If one admits that neuroblasts are endowed with chemotactic properties, then one might also imagine that they are capable of ameboid movements, initiated by factors secreted from epithelial, neural, or mesodermal elements. As a result, their processes may be oriented in the direction of chemical gradients, and thus guided to the secreting cells" (Ramon y Cajal 1892; trans. English, 1995).This surprisingly modern outlook emphasizing directed guidance was temporarily derailed by the views of Weiss during the 1920s and 1930s. He first argued that functional specificity did not arise as a consequence of specific axonal connections (Weiss 1936), and later argued that nonspecific mechanical guidance cues play a predominant role in guiding axons and organizing them into nerves and tracts

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Section: Substrata In Vivomentioning

confidence: 88%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

130

View full text Add to dashboard Cite

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“…Activity regulates growth cone responsiveness to guidance cues, enhancing netrin responsiveness and inhibiting myelin repulsion (Ming et al 2001). And, activity shapes the specificity of local connectivity of axons, for example in the selection and elimination of cortical innervation targets (Kalil et al 1986;Katz and Shatz 1996;Catalano and Shatz 1998). Data on the effect of activity on axon growth have been more controversial.…”

Section: Control Of Neuronal Responsiveness To Trophic Peptidesmentioning

confidence: 99%

How does an axon grow?

Goldberg¹

2003

Genes Dev.

204

138

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How do axons grow during development, and why do they fail to regrow when injured? In the complicated mesh of our nervous system, the axon is the information superhighway, carrying all of the data we use to sense our environment and carry out behaviors. To wire up our nervous system properly, neurons must elongate their axons during development to reach their targets. This is no simple task, however. The complex morphology of axons and dendrites puts neurons among the most intricate and beautiful cells in the body. Knowledge of how neurons extend axons and dendrites, elongate at a particular rate, and stop growing at the proper time is critical to understanding the development of our nervous system, yet the regulation of these processes is poorly understood. Considerable attention in recent years has focused on understanding how growth cones are guided and steered through complicated pathways (for review, see Schmidt and Hall 1998;Mueller 1999), and even how neurons initiate new processes (for review, see Da Silva and Dotti 2002), but what mechanisms are involved in elongation itself? Are environmental signals needed to drive axon growth and, if so, what are the intracellular molecular mechanisms by which they induce elongation? What controls the rate of axon growth? How do CNS neurons know whether to extend axons or dendrites? Is the signaling of axon versus dendrite growth attributable to different extracellular signals, different neuronal states, or both? All of these questions bear critically on our understanding of axon growth and here I review recent answers and approaches to the above questions, and highlight their relevance during development, injury, and disease.

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“…Axonal targeting and synapse formation are complex cellular processes, requiring that a neuron project along the correct pathway, choose the appropriate target, and construct and maintain a functional synapse (Tessier-Lavigne and Goodman, 1996). Although neuronal activity is involved in these processes (Catalano and Shatz, 1998;Ruthazer and Cline, 2004), recent evidence suggests that the formation of synapses may be more âhard-wiredâ than previously thought due to specific molecular cues (Jefferis et al, 2001;Clandinin and Zipursky, 2002;Ackley and Jin, 2004). A number of molecules have been identified to play a prominent role in axonal guidance, including semaphorins, ephrins, netrins, neurotrophins, and receptor protein tyrosine phosphatases.…”

Section: Introductionmentioning

confidence: 99%

The atypical cadherin flamingo regulates synaptogenesis and helps prevent axonal and synaptic degeneration in Drosophila

Bao

Berlanga

Xue

et al. 2007

Molecular and Cellular Neuroscience

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The formation of synaptic connections with target cells and maintenance of axons are highly regulated and crucial for neuronal function. The atypical cadherin and G-protein-coupled receptor Flamingo and its orthologs in amphibians and mammals have been shown to regulate cell polarity, dendritic and axonal growth, and neural tube closure. However, the role of Flamingo in synapse formation and function and in axonal health remains poorly understood. Here we show that fmi mutations cause a significant increase in the number of ectopic synapses on muscles and result in the formation of novel en passant synapses along axons, and unique presynaptic varicosities, including active zones, within axons. fmi mutations also cause defective synaptic responses in a small subset of muscles, an agedependent loss of muscle innervation and a drastic degeneration of axons in 3 rd instar larvae without an apparent loss of neurons. Neuronal expression of Flamingo rescues all of these synaptic and axonal defects and larval lethality. Based on these observations, we propose that Flamingo is required in neurons for synaptic target selection, synaptogenesis, the survival of axons and synapses, and adult viability. These findings shed new light on a possible role for Flamingo in progressive neurodegenerative diseases.

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Activity-Dependent Cortical Target Selection by Thalamic Axons

Cited by 249 publications

References 25 publications

Cellular Strategies of Axonal Pathfinding

Cellular Strategies of Axonal Pathfinding

How does an axon grow?

The atypical cadherin flamingo regulates synaptogenesis and helps prevent axonal and synaptic degeneration in Drosophila

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