Limits...
Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation.

Faucherre A, Pujol-Martí J, Kawakami K, López-Schier H - PLoS ONE (2009)

Bottom Line: Each neuron forms synapses with hair cells of identical orientation to divide the neuromast into functional planar-polarity compartments.We also show that afferent neurons are strict selectors of polarity that can re-establish synapses with identically oriented targets during hair-cell regeneration.Our results provide the anatomical bases for the physiological models of signal-polarity resolution by the lateral line.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Sensory Cell Biology & Organogenesis, Centre de Regulació Genòmica, Doctor Aiguader, Barcelona, Spain.

ABSTRACT
Hair cells in the inner ear display a characteristic polarization of their apical stereocilia across the plane of the sensory epithelium. This planar orientation allows coherent transduction of mechanical stimuli because the axis of morphological polarity of the stereocilia corresponds to the direction of excitability of the hair cells. Neuromasts of the lateral line in fishes and amphibians form two intermingled populations of hair cells oriented at 180 degrees relative to each other, however, creating a stimulus-polarity ambiguity. Therefore, it is unknown how these animals resolve the vectorial component of a mechanical stimulus. Using genetic mosaics and live imaging in transgenic zebrafish to visualize hair cells and neurons at single-cell resolution, we show that lateral-line afferents can recognize the planar polarization of hair cells. Each neuron forms synapses with hair cells of identical orientation to divide the neuromast into functional planar-polarity compartments. We also show that afferent neurons are strict selectors of polarity that can re-establish synapses with identically oriented targets during hair-cell regeneration. Our results provide the anatomical bases for the physiological models of signal-polarity resolution by the lateral line.

Show MeSH

Related in: MedlinePlus

Afferent innervation of adjacent neuromasts.(A–B) Maximal projections of single neurons labelled with mem-TdTomato innervating hair cells of the same polarity of (A) two adjacent neuromasts in an SqET4 transgenic fish and (B) three adjacent neuromasts in a brn3C∶GFP transgenic fish. Those depicted are the terminal neuromasts from a 4 dpf fish. Scale bar: 20 µm.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2637426&req=5

pone-0004477-g005: Afferent innervation of adjacent neuromasts.(A–B) Maximal projections of single neurons labelled with mem-TdTomato innervating hair cells of the same polarity of (A) two adjacent neuromasts in an SqET4 transgenic fish and (B) three adjacent neuromasts in a brn3C∶GFP transgenic fish. Those depicted are the terminal neuromasts from a 4 dpf fish. Scale bar: 20 µm.

Mentions: Mosaic expression of mem-TdTomato showed that some neurons innervate simultaneously two or three adjacent neuromasts (Figure 5). These neurons tended to be the longest: i.e., those that targeted the most caudal organs. We suspected that these neurons would contact hair cells of identical orientation in each neuromast. To test this hypothesis, we examined SqET4 and brn3c∶GFP stable transgenics expressing mem-TdTomato in single neurons. Because hair cells are born in pairs of opposite planar polarity along a single axis creating a line of mirror symmetry, all the cells located anterior to the line of symmetry are polarized posteriorly, whereas the posterior cells adopt an anterior orientation (Figure 4 D) [34]. Thus, the orientation of the hair cells can be predicted from their position with respect to the line of mirror symmetry. When the line of mirror symmetry was evident, we observed that bulged neurites established stable associations exclusively with hair cells on the same side of each neuromast. This indicates that each afferent neuron synapses with hair cells of identical orientation in adjacent neuromasts (Figure 5). Therefore, lateralis afferents can link several organs to form multi-neuromast sensory units.


Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation.

Faucherre A, Pujol-Martí J, Kawakami K, López-Schier H - PLoS ONE (2009)

Afferent innervation of adjacent neuromasts.(A–B) Maximal projections of single neurons labelled with mem-TdTomato innervating hair cells of the same polarity of (A) two adjacent neuromasts in an SqET4 transgenic fish and (B) three adjacent neuromasts in a brn3C∶GFP transgenic fish. Those depicted are the terminal neuromasts from a 4 dpf fish. Scale bar: 20 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2637426&req=5

pone-0004477-g005: Afferent innervation of adjacent neuromasts.(A–B) Maximal projections of single neurons labelled with mem-TdTomato innervating hair cells of the same polarity of (A) two adjacent neuromasts in an SqET4 transgenic fish and (B) three adjacent neuromasts in a brn3C∶GFP transgenic fish. Those depicted are the terminal neuromasts from a 4 dpf fish. Scale bar: 20 µm.
Mentions: Mosaic expression of mem-TdTomato showed that some neurons innervate simultaneously two or three adjacent neuromasts (Figure 5). These neurons tended to be the longest: i.e., those that targeted the most caudal organs. We suspected that these neurons would contact hair cells of identical orientation in each neuromast. To test this hypothesis, we examined SqET4 and brn3c∶GFP stable transgenics expressing mem-TdTomato in single neurons. Because hair cells are born in pairs of opposite planar polarity along a single axis creating a line of mirror symmetry, all the cells located anterior to the line of symmetry are polarized posteriorly, whereas the posterior cells adopt an anterior orientation (Figure 4 D) [34]. Thus, the orientation of the hair cells can be predicted from their position with respect to the line of mirror symmetry. When the line of mirror symmetry was evident, we observed that bulged neurites established stable associations exclusively with hair cells on the same side of each neuromast. This indicates that each afferent neuron synapses with hair cells of identical orientation in adjacent neuromasts (Figure 5). Therefore, lateralis afferents can link several organs to form multi-neuromast sensory units.

Bottom Line: Each neuron forms synapses with hair cells of identical orientation to divide the neuromast into functional planar-polarity compartments.We also show that afferent neurons are strict selectors of polarity that can re-establish synapses with identically oriented targets during hair-cell regeneration.Our results provide the anatomical bases for the physiological models of signal-polarity resolution by the lateral line.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Sensory Cell Biology & Organogenesis, Centre de Regulació Genòmica, Doctor Aiguader, Barcelona, Spain.

ABSTRACT
Hair cells in the inner ear display a characteristic polarization of their apical stereocilia across the plane of the sensory epithelium. This planar orientation allows coherent transduction of mechanical stimuli because the axis of morphological polarity of the stereocilia corresponds to the direction of excitability of the hair cells. Neuromasts of the lateral line in fishes and amphibians form two intermingled populations of hair cells oriented at 180 degrees relative to each other, however, creating a stimulus-polarity ambiguity. Therefore, it is unknown how these animals resolve the vectorial component of a mechanical stimulus. Using genetic mosaics and live imaging in transgenic zebrafish to visualize hair cells and neurons at single-cell resolution, we show that lateral-line afferents can recognize the planar polarization of hair cells. Each neuron forms synapses with hair cells of identical orientation to divide the neuromast into functional planar-polarity compartments. We also show that afferent neurons are strict selectors of polarity that can re-establish synapses with identically oriented targets during hair-cell regeneration. Our results provide the anatomical bases for the physiological models of signal-polarity resolution by the lateral line.

Show MeSH
Related in: MedlinePlus