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Curr Biol. 2014 Dec 15;24(24):2968-74. doi: 10.1016/j.cub.2014.11.012. Epub 2014 Dec 4.

Converging axons collectively initiate and maintain synaptic selectivity in a constantly remodeling sensory organ.

Author information

1
Unit of Sensory Biology & Organogenesis, Helmholtz Zentrum München, Ingolstädter Landstraße 1, 85764 Munich, Germany.
2
Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain.
3
Department of Biology and Neuroscience Program, Amherst College, Amherst, MA 01002-5000, USA.
4
Institute for Research in Biomedicine, Baldiri Reixac 10, 08028 Barcelona, Spain.
5
Unit of Sensory Biology & Organogenesis, Helmholtz Zentrum München, Ingolstädter Landstraße 1, 85764 Munich, Germany; Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain. Electronic address: hernan.lopez-schier@helmholtz-muenchen.de.

Abstract

Sensory receptors are the functional link between the environment and the brain. The repair of sensory organs enables animals to continuously detect environmental stimuli. However, receptor cell turnover can affect sensory acuity by changing neural connectivity patterns. In zebrafish, two to four postsynaptic lateralis afferent axons converge into individual peripheral mechanosensory organs called neuromasts, which contain hair cell receptors of opposing planar polarity. Yet, each axon exclusively synapses with hair cells of identical polarity during development and regeneration to transmit unidirectional mechanical signals to the brain. The mechanism that governs this exceptionally accurate and resilient synaptic selectivity remains unknown. We show here that converging axons are mutually dependent for polarity-selective connectivity. If rendered solitary, these axons establish simultaneous functional synapses with hair cells of opposing polarities to transmit bidirectional mechanical signals. Remarkably, nonselectivity by solitary axons can be corrected upon the reintroduction of additional axons. Collectively, our results suggest that lateralis synaptogenesis is intrinsically nonselective and that interaxonal interactions continuously rectify mismatched synapses. This dynamic organization of neural connectivity may represent a general solution to maintain coherent synaptic transmission from sensory organs undergoing frequent variations in the number and spatial distribution of receptor cells.

PMID:
25484295
DOI:
10.1016/j.cub.2014.11.012
[Indexed for MEDLINE]
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