scholarly journals Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Melinda S Modrell ◽  
Mike Lyne ◽  
Adrian R Carr ◽  
Harold H Zakon ◽  
David Buckley ◽  
...  
Keyword(s):  
Transcription Factor ◽  
Hair Cell ◽  
Lateral Line ◽  
Glutamate Release ◽  
Cell Types ◽  
Lateral Line System ◽  
Organ Development ◽  
Line System ◽  
Evolutionary Diversification ◽  
Ampullary Organ

The anamniote lateral line system, comprising mechanosensory neuromasts and electrosensory ampullary organs, is a useful model for investigating the developmental and evolutionary diversification of different organs and cell types. Zebrafish neuromast development is increasingly well understood, but neither zebrafish nor Xenopus is electroreceptive and our molecular understanding of ampullary organ development is rudimentary. We have used RNA-seq to generate a lateral line-enriched gene-set from late-larval paddlefish (Polyodon spathula). Validation of a subset reveals expression in developing ampullary organs of transcription factor genes critical for hair cell development, and genes essential for glutamate release at hair cell ribbon synapses, suggesting close developmental, physiological and evolutionary links between non-teleost electroreceptors and hair cells. We identify an ampullary organ-specific proneural transcription factor, and candidates for the voltage-sensing L-type Cav channel and rectifying Kv channel predicted from skate (cartilaginous fish) ampullary organ electrophysiology. Overall, our results illuminate ampullary organ development, physiology and evolution.

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

2018 ◽  
Vol 58 (2) ◽  
pp. 329-340 ◽  
Author(s):  
Clare V H Baker ◽  
Melinda S Modrell
Keyword(s):  
Gene Expression ◽  
Hair Cell ◽  
Electric Fields ◽  
Lateral Line ◽  
Hair Cells ◽  
Water Movement ◽  
Low Frequency ◽  
Lateral Line System ◽  
Line System ◽  
Ribbon Synapses

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.

Temporal precision and reliability in the velocity regime of a hair-cell sensory system: the mechanosensory lateral line of goldfish, Carassius auratus

2012 ◽  
Vol 107 (10) ◽  
pp. 2581-2593 ◽  
Author(s):  
Julie Goulet ◽  
J. Leo van Hemmen ◽  
Sarah N. Jung ◽  
Boris P. Chagnaud ◽  
Björn Scholze ◽  
...  
Keyword(s):  
Boundary Layer ◽  
Hair Cell ◽  
Lateral Line ◽  
Signal Reconstruction ◽  
Sensory System ◽  
Time Shift ◽  
Lateral Line System ◽  
Theoretic Approach ◽  
Free Standing ◽  
Line System

Fish and aquatic frogs detect minute water motion by means of a specialized mechanosensory system, the lateral line. Ubiquitous in fish, the lateral-line system is characterized by hair-cell based sensory structures across the fish's surface called neuromasts. These neuromasts occur free-standing on the skin as superficial neuromasts (SN) or are recessed into canals as canal neuromasts. SNs respond to rapid changes of water velocity in a small layer of fluid around the fish, including the so-called boundary layer. Although omnipresent, the boundary layer's impact on the SN response is still a matter of debate. For the first time using an information-theoretic approach to this sensory system, we have investigated the SN afferents encoding capabilities. Combining covariance analysis, phase analysis, and modeling of recorded neuronal responses of primary lateral line afferents, we show that encoding by the SNs is adequately described as a linear, velocity-responsive mechanism. Afferent responses display a bimodal distribution of opposite Wiener kernels that likely reflected the two hair-cell populations within a given neuromast. Using frozen noise stimuli, we further demonstrate that SN afferents respond in an extremely precise manner and with high reproducibility across a broad frequency band (10–150 Hz), revealing that an optimal decoder would need to rely extensively on a temporal code. This was further substantiated by means of signal reconstruction of spike trains that were time shifted with respect to their original. On average, a time shift of 3.5 ms was enough to diminish the encoding capabilities of primary afferents by 70%. Our results further demonstrate that the SNs' encoding capability is linearly related to the stimulus outside the boundary layer, and that the boundary layer can, therefore, be neglected while interpreting lateral line response of SN afferents to hydrodynamic stimuli.

scholarly journals Sox2 and Sox3 are essential for development and regeneration of the zebrafish lateral line

2019 ◽  
Author(s):  
Cristian A. Undurraga ◽  
Yunzi Gou ◽  
Pablo C. Sandoval ◽  
Viviana A. Nuñez ◽  
Miguel L. Allende ◽  
...  
Keyword(s):  
Stem Cells ◽  
Lateral Line ◽  
Hair Cells ◽  
Topological Analysis ◽  
Time Lapse ◽  
Cell Types ◽  
Lateral Line System ◽  
Loss Of Function ◽  
Supporting Cells ◽  
Line System

ABSTRACTThe recovery of injured or lost sensory neurons after trauma, disease or aging is a major scientific challenge. Upon hearing loss or balance disorder, regeneration of mechanosensory hair cells has been observed in fish, some amphibians and under special circumstances in birds, but is absent in adult mammals. In aquatic vertebrates, hair cells are not only present in the inner ear but also in neuromasts of the lateral line system. The zebrafish lateral line neuromast has an almost unlimited capacity to regenerate hair cells. This remarkable ability is possible due to the presence of neural stem/progenitor cells within neuromasts. In order to further characterize these stem cells, we use the expression of the neural progenitor markers Sox2 and Sox3, transgenic reporter lines, and morphological and topological analysis of the different cell types within the neuromast. We reveal new sub-populations of supporting cells, the sustentacular supporting cells and the neuromast stem cells. In addition, using loss-of-function and mutants of sox2 and sox3, we find that the combined activity of both genes is essential for lateral line development and regeneration. The capability of sox2/sox3 expressing stem cells to produce new hair cells, hair cell-precursors, and supporting cells after damage was analyzed in detail by time-lapse microscopy and immunofluorescence. We are able to provide evidence that sox2/3 expressing cells are the main contributors to the regenerated neuromast, and that their daughter cells are able to differentiate into most cell types of the neuromast.

From artificial hair cell sensor to artificial lateral line system: Development and application

2007 ◽  
Author(s):  
Yingchen Yang ◽  
Nannan Chen ◽  
Craig Tucker ◽  
Jonathan Engel ◽  
Saunvit Pandya ◽  
...  
Keyword(s):  
Hair Cell ◽  
Lateral Line ◽  
System Development ◽  
Lateral Line System ◽  
Line System

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

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.

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.

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