scholarly journals Using light-sheet microscopy to study spontaneous activity in the developing lateral-line system

2021 ◽  
Author(s):  
Qiuxiang Zhang ◽  
Katie Kindt

Hair cells are the sensory receptors in the auditory and vestibular systems of all vertebrates, and in the lateral-line system of aquatic vertebrates. During development, spontaneous activity in hair cells shapes the formation of these sensory systems. In auditory hair cells of mice, coordinated waves of spontaneous activity can be triggered by concomitant activity in nearby supporting cells. But in mammals, developing auditory and vestibular hair cells can also autonomously generate spontaneous events independent of supporting cell activity. To date, significant progress has been made studying spontaneous activity in the auditory and vestibular systems of mammals, in isolated cultures. The purpose of this work is to explore the zebrafish lateral-line system as a model to study and understand spontaneous activity in vivo. Our work applies genetically encoded calcium indicators along with light-sheet fluorescence microscopy to visualize spontaneous calcium activity in the developing lateral-line system. Consistent with our previous work, we show that spontaneous calcium activity is present in developing lateral-line hair cells. We now show that supporting cells that surround hair cells, and cholinergic efferent terminals that directly contact hair cells are also spontaneously active. Using two-color functional imaging we demonstrate that spontaneous activity in hair cells does not correlate with activity in either supporting cells or cholinergic terminals. We find that during lateral-line development, hair cells autonomously generate spontaneous events. Using localized calcium indicators, we show that within hair cells, spontaneous calcium activity occurs in two distinct domains-the mechanosensory bundle and the presynapse. Further, spontaneous activity in the mechanosensory bundle ultimately drives spontaneous calcium influx at the presynapse. Comprehensively, our results indicate that in developing lateral-line hair cells, autonomously generated spontaneous activity originates with spontaneous mechanosensory events. Overall, with robust spontaneous activity three different cell types, the developing lateral line is a rich model to study these activities in an intact sensory organ. Future work studying this model may further our understanding of these activities and their role in sensory system formation, function and regeneration.

2019 ◽  
Author(s):  
Cristian A. Undurraga ◽  
Yunzi Gou ◽  
Pablo C. Sandoval ◽  
Viviana A. Nuñez ◽  
Miguel L. Allende ◽  
...  

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.


2002 ◽  
Vol 329 (2) ◽  
pp. 133-136 ◽  
Author(s):  
F Abbate ◽  
S Catania ◽  
A Germanà ◽  
T González ◽  
B Diaz-Esnal ◽  
...  

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

2009 ◽  
Vol 5 (4) ◽  
pp. 477-479 ◽  
Author(s):  
M.J. McHenry ◽  
K.E. Feitl ◽  
J.A. Strother ◽  
W.J. Van Trump

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.


2018 ◽  
Vol 58 (2) ◽  
pp. 329-340 ◽  
Author(s):  
Clare V H Baker ◽  
Melinda S Modrell

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.


1950 ◽  
Vol 34 (1) ◽  
pp. 1-8 ◽  
Author(s):  
E. E. Suckling ◽  
J. A. Suckling

1. The lateral line of Fundulus heteroclitus and Fundulus majalis is shown to react to tone at an intensity level of 20 dynes per sq. cm. at frequencies up to 200 or 300 cycles per second. 2. Evidence is given that the nerve can reproduce the stimulating tone frequency up to at least 180 cycles per second. 3. The response of the lateral line to the swimming movements of nearby fish is demonstrated. 4. Fundulus and several other species are shown to give strong spontaneous activity of the lateral line nerve.


2004 ◽  
Vol 365 (3) ◽  
pp. 186-189 ◽  
Author(s):  
A Germana ◽  
F Abbate ◽  
T González-Martı́nez ◽  
M.E del Valle ◽  
F de Carlos ◽  
...  

1996 ◽  
Vol 199 (4) ◽  
pp. 893-899 ◽  
Author(s):  
J Montgomery ◽  
D Bodznick ◽  
M Halstead

Recordings were made from primary afferent fibres and secondary projection neurones (crest cells) in the mechanosensory lateral line system of the dwarf scorpionfish. Crest cells were identified by antidromic stimulation from the contralateral midbrain. Differences between primary afferent fibre and crest cell response characteristics are indicative of signal processing by the neuronal circuitry of the medial octavolateralis nucleus. There are a number of differences between primary afferent fibres and crest cells. Primary afferents have relatively high levels of spontaneous activity (mean close to 40 impulses s-1) and many of them are strongly modulated by ventilation. By contrast, crest cells have a much lower rate of spontaneous activity that is not obviously modulated by ventilation. Primary afferents show a simple tonic response to a maintained stimulus, whereas crest cells show a variety of temporal response properties, but in general show a phasic/tonic response to the same prolonged stimulus. Afferents are most sensitive to frequencies of stimulation around 100 Hz; in contrast, crest cells show a strong suppression of activity at this frequency. Crest cells are most responsive around 50 Hz. These afferent/secondary comparisons show similarities with those reported for allied electrosensory and auditory pathways.


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