scholarly journals Directional selectivity of afferent neurons in zebrafish neuromasts is regulated by Emx2 in presynaptic hair cells

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Young Rae Ji ◽  
Sunita Warrier ◽  
Tao Jiang ◽  
Doris K Wu ◽  
Katie S Kindt
Keyword(s):  
Hair Cells ◽  
Hair Bundle ◽  
Afferent Neuron ◽  
Lateral Line System ◽  
Directional Selectivity ◽  
Afferent Neurons ◽  
Line System ◽  
Sensory Hair Cells ◽  
Innervation Patterns ◽  
Hair Bundles

The orientation of hair bundles on top of sensory hair cells (HCs) in neuromasts of the lateral line system allows fish to detect direction of water flow. Each neuromast shows hair bundles arranged in two opposing directions and each afferent neuron innervates only HCs of the same orientation. Previously, we showed that this opposition is established by expression of Emx2 in half of the HCs, where it mediates hair bundle reversal (<xref ref-type="bibr" rid="bib15">Jiang et al., 2017</xref>). Here, we show that Emx2 also regulates neuronal selection: afferent neurons innervate either Emx2-positive or negative HCs. In emx2 knockout and gain-of-function neuromasts, all HCs are unidirectional and the innervation patterns and physiological responses of the afferent neurons are dependent on the presence or absence of Emx2. Our results indicate that Emx2 mediates the directional selectivity of neuromasts by two distinct processes: regulating hair bundle orientation in HCs and selecting afferent neuronal targets.

Ultrastructure of superficial neuromasts in the mottled sculpin, Cottus bairdi

1989 ◽  
Vol 47 ◽  
pp. 958-959
Author(s):  
W.R. Jones ◽  
S. Coombs ◽  
J. Janssen
Keyword(s):  
Hair Cells ◽  
Lateral Line System ◽  
Electron Microscopic ◽  
Line System ◽  
Dense Cores ◽  
Sensory Hair Cells ◽  
Cytoplasmic Vesicles ◽  
Cottus Bairdi ◽  
Mottled Sculpin ◽  
Upper Third

The lateral line system of the mottled sculpin, like that of most bony fish, has both canal (CNM) and superficial (SNM) sensory end organs, neuromasts, which are distributed on the head and trunk in discrete, readily identifiable groupings (Fig. 1). CNM and SNM differ grossly in location and in overall size and shape. The former are located in subdermal canals and are larger and asymmetric in shape, The latter are located directly on the surface of the skin and are much smaller and more symmetrical It has been suggested that the two may differ at a more fundamental level in such functionally related parameters as extent of myelination of innervating fibers and the absence of efferent innervation in SNM. The present study addresses the validity of these last two features as distinguishing criteria by examining the structure of those SNM populations indicated in Fig. 1 at both the light and electron microscopic levels.All of the populations of SNM examined conform in general to previously published descriptions, consisting of a neuroepithelium composed of sensory hair cells, support cells and mantle cells, Several significant differences from these accounts have, however, emerged. Firstly, the structural composition of the innervating fibers is heterogeneous with respect to the extent of myelination. All SNM groups, with the possible exception of the TRrs and CFLs, possess both myelinated and unmyelinated fibers within the neuroepithelium proper (Fig. 2), just as do CNM. The extent of myelina- tion is quite variable, with some fibers sheath terminating just before crossing the neuroepithelial basal lamina, some just after and a few retaining their myelination all the way to the base of the hair cells in the upper third of the neuroepithelium. Secondly, all SNMs possess fibers that may, on the basis of ultrastructural criteria, be identified as efferent. Such fibers contained numerous cytoplasmic vesicles, both clear and with dense cores. In regions where such fibers closely apposed hair cells, subsynaptic cisternae were observed in the hair cell (Fig. 3).

scholarly journals Frequency response properties of primary afferent neurons in the posterior lateral line system of larval zebrafish

2015 ◽  
Vol 113 (2) ◽  
pp. 657-668 ◽  
Author(s):  
Rafael Levi ◽  
Otar Akanyeti ◽  
Aleksander Ballo ◽  
James C. Liao
Keyword(s):  
Lateral Line ◽  
Sine Wave ◽  
Afferent Neuron ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Primary Afferent Neurons ◽  
Primary Afferent ◽  
Line System ◽  
Response Properties ◽  
Larval Zebrafish

The ability of fishes to detect water flow with the neuromasts of their lateral line system depends on the physiology of afferent neurons as well as the hydrodynamic environment. Using larval zebrafish ( Danio rerio), we measured the basic response properties of primary afferent neurons to mechanical deflections of individual superficial neuromasts. We used two types of stimulation protocols. First, we used sine wave stimulation to characterize the response properties of the afferent neurons. The average frequency-response curve was flat across stimulation frequencies between 0 and 100 Hz, matching the filtering properties of a displacement detector. Spike rate increased asymptotically with frequency, and phase locking was maximal between 10 and 60 Hz. Second, we used pulse train stimulation to analyze the maximum spike rate capabilities. We found that afferent neurons could generate up to 80 spikes/s and could follow a pulse train stimulation rate of up to 40 pulses/s in a reliable and precise manner. Both sine wave and pulse stimulation protocols indicate that an afferent neuron can maintain their evoked activity for longer durations at low stimulation frequencies than at high frequencies. We found one type of afferent neuron based on spontaneous activity patterns and discovered a correlation between the level of spontaneous and evoked activity. Overall, our results establish the baseline response properties of lateral line primary afferent neurons in larval zebrafish, which is a crucial step in understanding how vertebrate mechanoreceptive systems sense and subsequently process information from the environment.

S-100 protein is a selective marker for sensory hair cells of the lateral line system in teleosts

2002 ◽  
Vol 329 (2) ◽  
pp. 133-136 ◽  
Author(s):  
F Abbate ◽  
S Catania ◽  
A Germanà ◽  
T González ◽  
B Diaz-Esnal ◽  
...  
Keyword(s):  
Lateral Line ◽  
Hair Cells ◽  
Lateral Line System ◽  
Selective Marker ◽  
Line System ◽  
Sensory Hair ◽  
Sensory Hair Cells ◽  
S 100

Labeling Hair Cells and Afferent Neurons in the Posterior Lateral-Line System of Zebrafish

2013 ◽  
Vol 2013 (12) ◽  
pp. pdb.prot079467-pdb.prot079467 ◽  
Author(s):  
K. Schuster ◽  
A. Ghysen
Keyword(s):  
Lateral Line ◽  
Hair Cells ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Line System ◽  
Posterior Lateral Line

scholarly journals ELMOD1 stimulates ARF6-GTP hydrolysis to stabilize apical structures in developing vestibular hair cells

2017 ◽  
Author(s):  
Jocelyn F. Krey ◽  
Rachel A. Dumont ◽  
Philip A. Wilmarth ◽  
Larry L. David ◽  
Kenneth R. Johnson ◽  
...  
Keyword(s):  
Hair Cells ◽  
Membrane Trafficking ◽  
Apical Membrane ◽  
Small Gtpase ◽  
Hair Bundle ◽  
Type I ◽  
Sensory Hair ◽  
Cuticular Plate ◽  
Sensory Hair Cells ◽  
Hair Bundles

AbstractSensory hair cells require control of physical properties of their apical plasma membranes for normal development and function. Members of the ARF small GTPase family regulate membrane trafficking and cytoskeletal assembly in many cells. We identified ELMOD1, a guanine nucleoside triphosphatase activating protein (GAP) for ARF6, as the most highly enriched ARF regulator in hair cells. To characterize ELMOD1 control of trafficking, we used a mouse strain lacking functional ELMOD1 (roundabout; rda). In rda/rda mice, cuticular plates of utricle hair cells initially formed normally, then degenerated after postnatal day 5 (P5); large numbers of vesicles invaded the compromised cuticular plate. Hair bundles initially developed normally, but the cell’s apical membrane lifted away from the cuticular plate, and stereocilia elongated and fused. Membrane trafficking in type I hair cells, measured by FM1-43 dye labeling, was altered in rda/rda mice. Consistent with the proposed GAP role for ELMOD1, the ARF6 GTP/GDP ratio was significantly elevated in rda/rda utricles as compared to controls, and the level of ARF6-GTP was correlated with the severity of the rda/rda phenotype. These results suggest that conversion of ARF6 to its GDP-bound form is necessary for final stabilization of the hair bundle.Significance StatementAssembly of the mechanically sensitive hair bundle of sensory hair cells requires growth and reorganization of apical actin and membrane structures. Hair bundles and apical membranes in mice with mutations in the Elmod1 gene degenerate after formation, suggesting that the ELMOD1 protein stabilizes these structures. We show that ELMOD1 is a GTPase-activating protein in hair cells for the small GTP-binding protein ARF6, known to participate in actin assembly and membrane trafficking. We propose that conversion of ARF6 into the GDP-bound form in the apical domain of hair cells is essential for stabilizing apical actin structures like the hair bundle and ensuring that the apical membrane forms appropriately around the stereocilia.

scholarly journals Transcription factor Emx2 controls stereociliary bundle orientation of sensory hair cells

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Tao Jiang ◽  
Katie Kindt ◽  
Doris K Wu
Keyword(s):  
Transcription Factor ◽  
Hair Cells ◽  
Mirror Image ◽  
Hair Bundle ◽  
Polarity Reversal ◽  
Lateral Line System ◽  
Apical Surface ◽  
Sensory Organs ◽  
Line System ◽  
Image Pattern

The asymmetric location of stereociliary bundle (hair bundle) on the apical surface of mechanosensory hair cells (HCs) dictates the direction in which a given HC can respond to cues such as sound, head movements, and water pressure. Notably, vestibular sensory organs of the inner ear, the maculae, exhibit a line of polarity reversal (LPR) across which, hair bundles are polarized in a mirror-image pattern. Similarly, HCs in neuromasts of the zebrafish lateral line system are generated as pairs, and two sibling HCs develop opposite hair bundle orientations. Within these sensory organs, expression of the transcription factor Emx2 is restricted to only one side of the LPR in the maculae or one of the two sibling HCs in neuromasts. Emx2 mediates hair bundle polarity reversal in these restricted subsets of HCs and generates the mirror-image pattern of the sensory organs. Downstream effectors of Emx2 control bundle polarity cell-autonomously via heterotrimeric G proteins.

Gentamicin is ototoxic to all hair cells in the fish lateral line system

2010 ◽  
Vol 261 (1-2) ◽  
pp. 42-50 ◽  
Author(s):  
William J. Van Trump ◽  
Sheryl Coombs ◽  
Kyle Duncan ◽  
Matthew J. McHenry
Keyword(s):  
Lateral Line ◽  
Hair Cells ◽  
Lateral Line System ◽  
Line System

scholarly journals Larval zebrafish rapidly sense the water flow of a predator's strike

2009 ◽  
Vol 5 (4) ◽  
pp. 477-479 ◽  
Author(s):  
M.J. McHenry ◽  
K.E. Feitl ◽  
J.A. Strother ◽  
W.J. Van Trump
Keyword(s):  
Water Flow ◽  
Lateral Line ◽  
Hair Cells ◽  
Escape Response ◽  
Neuromuscular Control ◽  
Lateral Line System ◽  
Line System ◽  
Novel Device ◽  
Larval Fishes ◽  
Mechanosensory Hair Cells

Larval fishes have a remarkable ability to sense and evade the feeding strike of a predator fish with a rapid escape manoeuvre. Although the neuromuscular control of this behaviour is well studied, it is not clear what stimulus allows a larva to sense a predator. Here we show that this escape response is triggered by the water flow created during a predator's strike. Using a novel device, the impulse chamber, zebrafish ( Danio rerio ) larvae were exposed to this accelerating flow with high repeatability. Larvae responded to this stimulus with an escape response having a latency (mode=13–15 ms) that was fast enough to respond to predators. This flow was detected by the lateral line system, which includes mechanosensory hair cells within the skin. Pharmacologically ablating these cells caused the escape response to diminish, but then recover as the hair cells regenerated. These findings demonstrate that the lateral line system plays a role in predator evasion at this vulnerable stage of growth in fishes.

scholarly journals Localization of Neurotrophin Specific Trk Receptors in Mechanosensory Systems of Killifish (Nothobranchius guentheri)

2021 ◽  
Vol 22 (19) ◽  
pp. 10411
Author(s):  
Marialuisa Aragona ◽  
Caterina Porcino ◽  
Maria Cristina Guerrera ◽  
Giuseppe Montalbano ◽  
Maria Levanti ◽  
...  
Keyword(s):  
Inner Ear ◽  
Hair Cells ◽  
S100 Protein ◽  
Sensory Systems ◽  
Sensory Cells ◽  
Lateral Line System ◽  
Suitable Model ◽  
Trk Receptors ◽  
Line System ◽  
Nothobranchius Guentheri

Neurotrophins (NTs) and their signal-transducing Trk receptors play a crucial role in the development and maintenance of specific neuronal subpopulations in nervous and sensory systems. NTs are supposed to regulate two sensory systems in fish, the inner ear and the lateral line system (LLS). The latter is one of the major mechanosensory systems in fish. Considering that annual fishes of the genus Nothobranchius, with their short life expectancy, have become a suitable model for aging studies and that the occurrence and distribution of neurotrophin Trk receptors have never been investigated in the inner ear and LLS of killifish (Nothobranchius guentheri), our study aimed to investigate the localization of neurotrophin-specific Trk receptors in mechanosensory systems of N. guentheri. For histological and immunohistochemical analysis, adult specimens of N. guentheri were processed using antibodies against Trk receptors and S100 protein. An intense immunoreaction for TrkA and TrkC was found in the sensory cells of the inner ear as well as in the hair cells of LLS. Moreover, also the neurons localized in the acoustic ganglia displayed a specific immunoreaction for all Trk receptors (TrkA, B, and C) analyzed. Taken together, our results demonstrate, for the first time, that neurotrophins and their specific receptors could play a pivotal role in the biology of the sensory cells of the inner ear and LLS of N. guentheri and might also be involved in the hair cells regeneration process in normal and aged conditions.

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