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 ◽  
...  

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.

Zoomorphology ◽  
2020 ◽  
Author(s):  
Harald Ahnelt ◽  
David Ramler ◽  
Maria Ø. Madsen ◽  
Lasse F. Jensen ◽  
Sonja Windhager

AbstractThe mechanosensory lateral line of fishes is a flow sensing system and supports a number of behaviors, e.g. prey detection, schooling or position holding in water currents. Differences in the neuromast pattern of this sensory system reflect adaptation to divergent ecological constraints. The threespine stickleback, Gasterosteus aculeatus, is known for its ecological plasticity resulting in three major ecotypes, a marine type, a migrating anadromous type and a resident freshwater type. We provide the first comparative study of the pattern of the head lateral line system of North Sea populations representing these three ecotypes including a brackish spawning population. We found no distinct difference in the pattern of the head lateral line system between the three ecotypes but significant differences in neuromast numbers. The anadromous and the brackish populations had distinctly less neuromasts than their freshwater and marine conspecifics. This difference in neuromast number between marine and anadromous threespine stickleback points to differences in swimming behavior. We also found sexual dimorphism in neuromast number with males having more neuromasts than females in the anadromous, brackish and the freshwater populations. But no such dimorphism occurred in the marine population. Our results suggest that the head lateral line of the three ecotypes is under divergent hydrodynamic constraints. Additionally, sexual dimorphism points to divergent niche partitioning of males and females in the anadromous and freshwater but not in the marine populations. Our findings imply careful sampling as an important prerequisite to discern especially between anadromous and marine threespine sticklebacks.


2017 ◽  
Vol 51 (5) ◽  
pp. 103-115 ◽  
Author(s):  
Kevin Nelson ◽  
Kamran Mohseni

AbstractThis paper presents a sensory system that is biologically inspired by the lateral line sensory system found in fish. This artificial lateral line system provides sensory information to be used in vehicle control algorithms, both to reduce model complexity and to measure hydrodynamic disturbances. The system presented in this paper is a modular implementation that can fit around a vehicle without requiring modifications to the hull. The design and manufacturing processes are presented in detail along with considerations for sensor placement and port spacing. An algorithm for calculating the hydrodynamic forces acting on the surface of a vehicle is derived and experimentally validated. An underwater motion capture system and strain sensors are used to calculate a reference hydrodynamic force that compares favorably with the hydrodynamic force calculated by the lateral line system.


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.


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.


2002 ◽  
Vol 88 (3) ◽  
pp. 1252-1262 ◽  
Author(s):  
Matthew S. Weeg ◽  
Andrew H. Bass

The mechanosensory lateral line of fish is a hair cell based sensory system that detects water motion using canal and superficial neuromasts. The trunk lateral line of the plainfin midshipman fish, Porichthys notatus, only has superficial neuromasts. The posterior lateral line nerve (PLLn) therefore innervates trunk superficial neuromasts exclusively and provides the opportunity to investigate the physiological responses of these receptors without the confounding influence of canal organs. We recorded single-unit activity from PLLn primary afferents in response to a vibrating sphere stimulus calibrated to produce an equal velocity across frequencies. Threshold tuning, isovelocity, and input/output curves were constructed using spike rate and vector strength, a measure of phase locking of spike times to the stimulus waveform. All units responded maximally to frequencies of 20–50 Hz. Units were classified as low-pass, band-pass, broadly tuned, or complex based on the shapes of tuning and isovelocity curves between 20 and 100 Hz. A 100 Hz stimulus caused an increase in spike rate in almost 50%, and significant synchronization in >80%, of all units. Midshipman vocalizations contain significant energy at and below 100 Hz, so these results demonstrate that the midshipman peripheral lateral line system can encode these acoustic signals. These results provide the first direct demonstration that units innervating superficial neuromasts in a teleost fish have heterogeneous frequency response properties, including an upper range of sensitivity that overlaps spectral peaks of behaviorally relevant acoustic stimuli.


Author(s):  
Yingchen Yang ◽  
Nannan Chen ◽  
Craig Tucker ◽  
Jonathan Engel ◽  
Saunvit Pandya ◽  
...  

Author(s):  
T. S. Kemp

‘The amphibians’ world’ focuses on the amphibians’ sense organs. Amphibians have the eyes, ears, olfactory organs of smell in the nose, and touch receptors common to all vertebrates, but the relative importance of the different senses varies from group to group depending on habitats and modes of life. Anurans have a sensory world most like that of humans; their vision is good, and includes the ability to see colours, and their hearing is acute. Urodeles and caecilians rely much more on their senses of smell and touch. Amphibian larvae have an additional sensory system called the lateral line system. Amphibians use several sensory cues in combination to navigate around their territories.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Melinda S Modrell ◽  
Mike Lyne ◽  
Adrian R Carr ◽  
Harold H Zakon ◽  
David Buckley ◽  
...  

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.


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