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The Journal of Neuroscience, August 20, 2008, 28(34):8442-8453; doi:10.1523/JNEUROSCI.2425-08.2008

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Development/Plasticity/Repair
Specificity of Afferent Synapses onto Plane-Polarized Hair Cells in the Posterior Lateral Line of the Zebrafish

Aaron Nagiel, Daniel Andor-Ardó, and A. J. Hudspeth

Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, New York, New York 10065-6399

Correspondence should be addressed to Dr. A. J. Hudspeth, Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, Campus Box 314, 1230 York Avenue, New York, NY 10065-6399. Email: hudspaj{at}rockefeller.edu

The proper wiring of the vertebrate brain represents an extraordinary developmental challenge, requiring billions of neurons to select their appropriate synaptic targets. In view of this complexity, simple vertebrate systems provide necessary models for understanding how synaptic specificity arises. The posterior lateral-line organ of larval zebrafish consists of polarized hair cells organized in discrete clusters known as neuromasts. Here we show that each afferent neuron of the posterior lateral line establishes specific contacts with hair cells of the same hair-bundle polarity. We quantify this specificity by modeling the neuron as a biased selector of hair-cell polarity and find evidence for bias from as early as 2.5 d after fertilization. More than half of the neurons form contacts on multiple neuromasts, but the innervated organs are spatially consecutive and the polarity preference is consistent. Using a novel reagent for correlative electron microscopy, HRP-mCherry, we show that these contacts are indeed afferent synapses bearing vesicle-loaded synaptic ribbons. Moreover, afferent neurons reassume their biased innervation pattern after hair-cell ablation and regeneration. By documenting specificity in the pattern of neuronal connectivity during development and in the context of organ regeneration, these results establish the posterior lateral-line organ as a vertebrate system for the in vivo study of synaptic target selection.

Key words: acousticolateralis system; eighth nerve; fluorescent protein; hair cell; planar cell polarity; ribbon synapse

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Received May 29, 2008; revised July 10, 2008; accepted July 11, 2008.

Correspondence should be addressed to Dr. A. J. Hudspeth, Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, Campus Box 314, 1230 York Avenue, New York, NY 10065-6399. Email: hudspaj{at}rockefeller.edu

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				A. Nagiel, S. H. Patel, D. Andor-Ardo, and A. J. Hudspeth Activity-independent specification of synaptic targets in the posterior lateral line of the larval zebrafish PNAS, December 22, 2009; 106(51): 21948 - 21953. [Abstract] [Full Text] [PDF]

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