Insights into Electroreceptor Development and Evolution from Molecular Comparisons with Hair Cells

Abstract The vertebrate lateral line system comprises a mechanosensory division, with neuromasts containing hair cells that detect local water movement (“distant touch”); and an electrosensory division, with electrosensory organs that detect the weak, low-frequency electric fields surrounding other animals in water (primarily used for hunting). The entire lateral line system was lost in the amniote lineage with the transition to fully terrestrial life; the electrosensory division was lost independently in several lineages, including the ancestors of frogs and of teleost fishes. (Electroreception with different characteristics subsequently evolved independently within two teleost lineages.) Recent gene expression studies in a non-teleost actinopterygian fish suggest that electroreceptor ribbon synapses employ the same transmission mechanisms as hair cell ribbon synapses, and show that developing electrosensory organs express transcription factors essential for hair cell development, including Atoh1 and Pou4f3. Previous hypotheses for electroreceptor evolution suggest either that electroreceptors and hair cells evolved independently in the vertebrate ancestor from a common ciliated secondary cell, or that electroreceptors evolved from hair cells. The close developmental and putative physiological similarities implied by the gene expression data support the latter hypothesis, i.e., that electroreceptors evolved in the vertebrate ancestor as a “sister cell-type” to lateral line hair cells.

Download Full-text

Design of a Microfluidic Device to Induce Noise Damage in Hair Cells of the Zebrafish Lateral Line

Volume 9: Micro- and Nano-Systems Engineering and Packaging, Parts A and B ◽

10.1115/imece2012-87135 ◽

2012 ◽

Author(s):

Hyuck-Jin Kwon ◽

Yuhao Xu ◽

Stephen A. Solovitz ◽

Wei Xue ◽

Alexander G. Dimitrov ◽

...

Keyword(s):

Hair Cell ◽

Flow Pattern ◽

Boundary Layers ◽

Microfluidic Device ◽

Lateral Line ◽

Hair Cells ◽

Cfd Simulation ◽

Lateral Line System ◽

Line System ◽

Noise Damage

Hearing loss affects millions of people worldwide and often results from death of the sensory hair cells in the inner ear. Noise-induced damage is one of the leading causes of hair cell loss. Recently, the zebrafish lateral line system has emerged as a powerful in vivo model for real-time studies of hair cell damage and protection. In this research, we designed a microfluidic device to induce noise damage in hair cells of the zebrafish lateral line. As the first step, a 3-D computational fluid dynamics (CFD) simulation was utilized to predict the flow pattern inside the device. An ideal flow pattern for our application should feature higher velocity at the side and lower velocity in the middle of a channel. Flow induced from ordinary channel geometry with single inlet/outlet pair would not work for us because the boundary layers from the two side walls will grow and merge with each other and induce the maximum flow speed in the middle of the channel. In order to achieve the desired flow pattern, side-wall inlet/outlet pairs were used to suppress the growth of boundary layers. CFD simulation was used to design important parameters such as dimensions of the microfluidic channel and the angle of inlets and outlets. It was found that flow velocity at the side of the channel could be 6.7 times faster than the velocity in the middle when we array the inlets and outlets alternatively and set the angle of the inlet to 45° with 2.0 mm main channel width. This 3-D CFD model will serve as a convenient model to design a microfluidic device to induce noise damage in hair cells of a zebrafish lateral line by manipulating the flow pattern inside the device.

Download Full-text

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

Neuroscience Letters ◽

10.1016/s0304-3940(02)00597-9 ◽

2002 ◽

Vol 329 (2) ◽

pp. 133-136 ◽

Cited By ~ 17

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

Download Full-text

Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system

Journal of Neuroscience ◽

10.1523/jneurosci.10-08-02502.1990 ◽

1990 ◽

Vol 10 (8) ◽

pp. 2502-2512 ◽

Cited By ~ 141

Author(s):

KJ Balak ◽

JT Corwin ◽

JE Jones

Keyword(s):

Laser Ablation ◽

Lateral Line ◽

Hair Cells ◽

Supporting Cell ◽

Lateral Line System ◽

Line System

Download Full-text

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

Hearing Research ◽

10.1016/j.heares.2010.01.001 ◽

2010 ◽

Vol 261 (1-2) ◽

pp. 42-50 ◽

Cited By ~ 62

Author(s):

William J. Van Trump ◽

Sheryl Coombs ◽

Kyle Duncan ◽

Matthew J. McHenry

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Lateral Line System ◽

Line System

Download Full-text

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

Biology Letters ◽

10.1098/rsbl.2009.0048 ◽

2009 ◽

Vol 5 (4) ◽

pp. 477-479 ◽

Cited By ~ 93

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.

Download Full-text

The mechanism of the lateral sense organs of fishes

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1937.0064 ◽

1937 ◽

Vol 123 (833) ◽

pp. 472-495 ◽

Cited By ~ 43

Keyword(s):

Lateral Line ◽

Cranial Nerves ◽

Sensory System ◽

Low Frequency ◽

Lateral Line System ◽

Sense Organs ◽

Line System ◽

Morphological Studies ◽

Low Frequency Vibration ◽

Functional Features

For a long time after their discovery in the seventeenth century the lateral-line canals of fishes were considered to be mucus-secreting organs. In 1850 Leydig described sense organs in the lateral-line canals, and this discovery stimulated a keen interest in the investigation of both the morphological and functional features of the lateral-line system. Morphological studies have yielded a thorough understanding of the structure of these organs (Ewart and Mitchell 1892; Cole 1896; Johnson 1917; von Woellwarth 1933). Physiological studies, though numerous, have been less fruitful. An account of the older work was given by Baglioni (1913), and the more recent work is reviewed by Dykgraaf (1933). The only technique until recently available has been the elimination of the sensory system by nerve section and cauterization, and the comparison of the behaviour of intact and operated fishes in response to various stimuli. With so diffuse a structure as the lateral-line system, receiving its nerve supply from the fifth, seventh, ninth and tenth cranial nerves, this method is particularly inadequate, and involves a violent mutilation of the animal. When one considers the crudity of many of these operations, it is not the uncertainty of the results which is remarkable, but rather that some of the conclusions reached should remain valid to-day in the light of far more penetrating experimental analysis. This method of organ elimination could yield at best only an indication of the kind of stimulus that is effective in evoking the excitation of lateral-line receptors. In current textbooks the conclusion of Parker (1904) that the effective stimulus for the lateral line is low-frequency vibration, and that of Hofer (1907) that it is movement of water (i. e. local currents) have received most notice. The observations of Dykgraaf (1933), who employed the more refined methods of von Frisch’s futterdressur technique, support Hofer’s conclusion, and to some extent also Parker’s. Dykgraaf considers the lateral-line system to be an organ of Ferntastsinn , and if this is taken to mean a mechanoreceptor of such sensitivity that it can function both as a touch organ and as a receptor for disturbances coming from a distance, it is undoubtedly a true description, for it is fully confirmed by the direct electrophysiological studies of Hoagland (1933 a, b, c and d ) and of Schriever (1935). The latter, apparently unacquainted with Hoagland’s work, did little more than to confirm several of his observations.

Download Full-text

The Inner Ear is Responsible for Detection of Infrasound in the Perch (Perca Fluviatilis)

Journal of Experimental Biology ◽

10.1242/jeb.171.1.163 ◽

1992 ◽

Vol 171 (1) ◽

pp. 163-172 ◽

Cited By ~ 1

Author(s):

HANSERIK KARLSEN

Keyword(s):

Inner Ear ◽

Lateral Line ◽

Low Frequency ◽

Perca Fluviatilis ◽

Lateral Line System ◽

Threshold Values ◽

Line System ◽

Frequency Detection ◽

Perch Perca Fluviatilis ◽

Cardiac Conditioning

In a previous study of infrasound detection in the cod, the inner ear was suggested to be the sensory organ responsible for the responses. However, a possible involvement of the lateral-line system in the observed low-frequency detection could not be ruled out. The infrasound sensitivity was therefore studied in perch (Perca fluviatilis) with normal and blocked lateral-line organs. The experiments were performed using a standing wave acoustic tube and the cardiac conditioning technique. All perch readily responded to infrasound frequencies down to 0.3 Hz with threshold values of approximately 2×10−4 ms−2. These thresholds were not affected by complete blocking of the lateral-line system with Co2+, which suggests that the inner ear is responsible for the observed infrasound detection by the perch.

Download Full-text

Research on an Artificial Lateral Line System Based on a Bionic Hair Sensor with Resonant Readout

Micromachines ◽

10.3390/mi10110736 ◽

2019 ◽

Vol 10 (11) ◽

pp. 736 ◽

Cited By ~ 2

Author(s):

Yang ◽

Zhang ◽

Liang ◽

Keyword(s):

Flow Velocity ◽

Lateral Line ◽

Gas Flow ◽

Air Flow ◽

Low Frequency ◽

Lateral Line System ◽

Least Mean Square ◽

Line System ◽

Canal Neuromast ◽

Air Flow Velocity

Inspired by the lateral line system of fish, an artificial lateral line system based on bionic hair sensor with resonant readout is presented in this paper. An artificial lateral line system, which possesses great application potential in the field of gas flow visualization, includes two different sensors: a superficial neuromast and a canal neuromast flow velocity sensor, which are used to measure the constant and oscillatory air flow velocity, respectively. The sensitive mechanism of two artificial lateral line sensors is analyzed, and a finite element simulation is implemented to verify the structural design. Then the control circuit of the artificial lateral line system is designed, employing a demodulation algorithm of oscillatory signal based on the least mean square error algorithm, which is used to calculate the oscillatory air flow velocity. Finally, the experiments are implemented to assess the performance of the two artificial lateral line systems. The experimental results show that the artificial lateral line system, which can be used to measure the constant and oscillatory air flow velocity, has a minimum threshold of 0.785 mm/s in the measurement of oscillatory air flow velocity. Moreover, the artificial canal neuromast lateral line system can filter out low-frequency disturbance and has good sensitivity for high-frequency flow velocity.

Download Full-text

Neural transduction in Xenopus laevis lateral line system

Journal of Neurophysiology ◽

10.1152/jn.1978.41.2.432 ◽

1978 ◽

Vol 41 (2) ◽

pp. 432-444 ◽

Cited By ~ 39

Author(s):

D. Strelioff ◽

V. Honrubia

Keyword(s):

Hair Cell ◽

Lateral Line ◽

Hair Cells ◽

Water Movement ◽

Neural Response ◽

Neural Responses ◽

Cell Systems ◽

Afferent Fibers ◽

Neural Excitation ◽

Electrical Stimuli

1. The process of neural excitation in hair cell systems was studied in an in vitro preparation of the Xenopus laevis (African clawed toad) lateral line organ. A specially designed stimulus chamber was used to apply accurately controlled pressure, water movement, or electrical stimuli, and to record the neural responses of the two afferent fibers innervating each organ or stitch. The objective of the study was to determine the characteristics of the neural responses to these stimuli, and thus gain insight into the transduction process. 2. A sustained deflection of the hair cell cilia due to a constant flow of water past the capula resulted in a maintained change in the mean firing rate (MFR) of the afferent fibers. The data also demonstrated that the neural response was proportional to the velocity of the water flow and indicated that both deflection and movement of the cilia were the effective physiological stimuli for this hair cell system. 3. The preparations responded to sinusoidal water movements (past the capula) over the entire frequency range of the stimulus chamber, 0.1-130 Hz, and were most sensitive between 10 and 40 Hz. The variation of the MFR and the percent modulation indicated that the average dynamic range of each organ was 23.5 dB. 4. The thresholds, if any, for sustained pressure changes and for sinusoidal pressure variations in the absence of water movements were very high. Due to the limitations of the stimulus chamber it was not possible to generate pressure stimuli of sufficient magnitude to elicit a neural response without also generating suprathreshold water-movement stimuli. Sustained pressures had no detectable effect on the neural response to water-movement stimuli. 5. The preparations were very sensitive to electrical potentials applied across the toad skin on which the hair cells were located. Potentials which made the ciliated surfaces of the hair cells positive with respect to their bases increased the MFR of the fibers, whereas negative potentials decreased it. The responses to sinusoidal electrical stimuli were similar to responses to water-movement stimuli with respect to frequency and dynamic ranges. Thresholds as low as 100 muV peak to peak (p-p) for 16-Hz stimuli were found. 6. The characteristics of the neural responses to electrical stimulation as well as supporting data obtained from the studies of the effects of anoxia on the evoked responses indicate that the electrical stimulus acts on the hair cells or on the synapses, rather than directly on the nerve fibers. This finding suggests that receptor potentials or their associated currents play an important role in the process of neural excitation in hair cell systems.

Download Full-text