PUBLICATION

Multispectral four-dimensional imaging reveals that evoked activity modulates peripheral arborization and the selection of plane-polarized targets by sensory neurons

Authors

Faucherre, A., Baudoin, J.P., Pujol-Martí, J., and Lopez-Schier, H.

ID

ZDB-PUB-100504-14

Date

2010

Source

Development (Cambridge, England) 137(10): 1635-1643 (Journal)

Registered Authors

Faucherre, Adele, Lopez-Schier, Hernan, Marti, Jesus Pujol

Keywords

Hair cells, Planar polarity, Regeneration, Sensory neurons, Deafness, Zebrafish

MeSH Terms

Evoked Potentials/physiology*
Synaptic Transmission/physiology
Models, Biological
Zebrafish/embryology*
Zebrafish/physiology
Sensory Receptor Cells/physiology*
Body Patterning/physiology*
Imaging, Three-Dimensional/methods
Animals
Deafness/embryology
Deafness/etiology
Mechanotransduction, Cellular/physiology
Cell Differentiation/physiology
Lateral Line System/embryology*
Lateral Line System/physiology
Hair Cells, Auditory/physiology
Animals, Genetically Modified
Microscopy, Fluorescence/methods

(all 18)

PubMed

20430744 Full text @ Development

Abstract

The polarity of apical stereocilia endows hair cells with directional excitability, which in turn enables animals to determine the vectorial component of a sound. Neuromasts of the lateral line of aquatic vertebrates harbor two populations of hair cells that are oriented at 180 degrees relative to each other. The resulting sensory-vectorial ambiguity is solved by lateralis afferent neurons that discriminate between hair cells of opposite polarities to innervate only those with the same orientation. How neurons select identically oriented hair cells remains unknown. To gain insight into the mechanism that underlies this selection, we devised a simple method to gather dynamic morphometric information about axonal terminals in toto by four-dimensional imaging. Applying this strategy to the zebrafish allowed us to correlate hair cell orientation to single afferent neurons at subcellular resolution. Here we show that in zebrafish with absent hair cell mechanoreception, lateralis afferents arborize profusely in the periphery, display less stability, and make improper target selections. Central axons, however, show no dynamic changes and establish normal contacts with the Mauthner cell, a characteristic second-order target in the hindbrain. We propose that the hardwired developmental mechanisms that underlie peripheral arborization and target recognition are modulated by evoked hair cell activity. This interplay between intrinsic and extrinsic cues is essential for plane-polarized target selection by lateralis afferent neurons.

Genes / Markers

Figures

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Expression

Gene	Fish	Conditions	Stage	Anatomy	Assay	Figure
EGFP	cntnap2a^nkhgn39dEt	standard conditions	Days 7-13	afferent neuron neuron projection	IFL	Fig. 1
EGFP	cntnap2a^nkhgn39dEt	standard conditions	Days 7-13	posterior lateral line ganglion	IFL	Fig. 1
GFP	rw0130aTg; rw0Tg	standard conditions	Days 7-13	efferent neuron neuron projection	IFL	Fig. 1
GFP	s356tTg	standard conditions	Days 7-13	neuromast hair cell	IFL	Fig. 1
GFP	s356tTg	standard conditions	Days 7-13	neuromast hair cell	IFL	Fig. 2
GFP	s356tTg	standard conditions	Days 7-13	neuromast hair cell	IFL	Fig. 6
GFP	tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	inner ear neuron projection	IFL	Fig. 5
GFP	tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	neuromast hair cell	IFL	Fig. 6
GFP	tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	neuromast hair cell	IFL	Fig. 2
Kaede	rw0130aTg; rw0Tg	standard conditions	Days 7-13	lateral line afferent neuron	IFL	Fig. 1

1 - 10 of 11

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Phenotype

Fish	Conditions	Stage	Phenotype	Figure
WT + MO1-cdh23	standard conditions	Day 4	afferent neuron has extra parts of type afferent neuron neuron projection, abnormal	Fig. S2
WT + MO1-cdh23	standard conditions	Day 4	afferent neuron neuron projection complexity, abnormal	Fig. S2
WT + MO1-cdh23	standard conditions	Day 4	afferent neuron neuron projection development process quality, abnormal	Fig. S2
WT + MO1-cdh23	standard conditions	Day 4	afferent neuron neuron projection transient, abnormal	Fig. S2
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron has extra parts of type afferent neuron dendritic branch, abnormal	Fig. 2
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron has extra parts of type afferent neuron neuron projection, abnormal	Fig. 2
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron has extra parts of type afferent neuron neuron projection, abnormal	Fig. 1
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron neuron projection complexity, abnormal	Fig. 2
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron neuron projection development process quality, abnormal	Fig. 4
tmie^{ru1000/ru1000}; s356tTg	standard conditions	Days 7-13	afferent neuron neuron projection transient, abnormal	Fig. 4

1 - 10 of 10

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Mutations / Transgenics

Allele	Construct	Type	Affected Genomic Region
nkhgn39dEt	Et(T2KHG)	Transgenic Insertion	cntnap2a
ru1000		Indel	tmie
rw0Tg	Tg(isl1a:GFP)	Transgenic Insertion
rw0130aTg	Tg(elavl3:Kaede)	Transgenic Insertion
s356tTg	Tg(pou4f3:GAP-GFP)	Transgenic Insertion

1 - 5 of 5

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Human Disease / Model

Sequence Targeting Reagents

Target	Reagent	Reagent Type
cdh23	MO1-cdh23	MRPHLNO

Fish

Fish
cntnap2a^nkhgn39dEt
rw0Tg
rw0130aTg
rw0130aTg; rw0Tg
s356tTg
tmie^{ru1000/ru1000}
tmie^{ru1000/ru1000}; s356tTg
WT + MO1-cdh23

Antibodies

Name	Type	Antigen Genes	Isotypes	Host Organism
Ab1-ctbp2l	polyclonal	ctbp2l		Rabbit

Orthology

Engineered Foreign Genes

Marker	Marker Type	Name
EGFP	EFG	EGFP
GFP	EFG	GFP
Kaede	EFG	Kaede

Mapping

Faucherre et al., 2010 ZDB-PUB-100504-14 PMID:20430744

Multispectral four-dimensional imaging reveals that evoked activity modulates peripheral arborization and the selection of plane-polarized targets by sensory neurons

Faucherre et al., 2010

ZDB-PUB-100504-14
PMID:20430744