Lateral-line activity during undulatory body motions suggests a feedback link in closed-loop control of sea lamprey swimming

2009 ◽  
Vol 87 (8) ◽  
pp. 671-683 ◽  
Author(s):  
A. Ayali ◽  
S. Gelman ◽  
E. D. Tytell ◽  
A. H. Cohen

The lateral-line system is common to most aquatic organisms. It plays an important role in behaviours involving detection of other animals and obstacles. In gnathostome fishes, these behaviours appear to be dependent on an efferent inhibitory system that filters out stimuli caused by the animal’s own movement. Sea lampreys ( Petromyzon marinus L., 1758), the most basal extant vertebrate, possess a functional lateral-line system. Yet they completely lack the inhibitory efferent system. Thus, they may use the lateral line to sense their own swimming movements, helping to stabilize swimming. To test this hypothesis, we first investigated the kinematics of free-swimming lampreys. In an intact tethered preparation, we then generated undualatory body motions of comparable amplitude and frequency to swimming, while monitoring the evoked responses of the posterior lateral-line nerve. Last, we tested the effect of eliminating lateral-line inputs by cobalt treatment. In the tethered preparation, we recorded distinctive and consistent activity in the lateral-line nerve that was strongly dependent on characteristics of the motion. We found that distinct characteristics of the rhythmic movements are encoded in the temporal characteristics of the response. Swimming kinematics of cobalt-treated animals differed from controls, suggesting a complex, yet necessary role of the lateral-line system in closed-loop control of swimming.

2015 ◽  
Vol 10 (2) ◽  
pp. 025002 ◽  
Author(s):  
Levi DeVries ◽  
Francis D Lagor ◽  
Hong Lei ◽  
Xiaobo Tan ◽  
Derek A Paley

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.


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.


1995 ◽  
Vol 198 (12) ◽  
pp. 2581-2591 ◽  
Author(s):  
T G Deliagina ◽  
F Ullén ◽  
M-J. Gonzalez ◽  
H Ehrsson ◽  
G N Orlovsky ◽  
...  

The lateral line system of lampreys includes photoreceptors distributed in the skin of the tail region. These are innervated by the trunk lateral line nerves, and the afferents terminate bilaterally in the medial octavolateral nucleus, crossing the midline through the cerebellar commissure. Stimulation of the dermal photoreceptors by tail illumination initiates locomotion. The present study was performed to characterize the response to illumination in larval and adult lampreys in detail and to elucidate the neuronal pathways responsible for the activation of locomotion. In both larval and adult quiescent lampreys, the response to unilateral illumination of the tail was found to consist of an initial turn followed by rectilinear swimming. The sign and magnitude of the turning angle were not correlated with the laterality of the optic stimulus. In mechanically restrained lampreys, spinalized at the level of segments 15­20, tail illumination evoked a complex motor response in the rostral part of the body, with switches between different patterns of coordination (turns in different directions, locomotion, and turns combined with locomotion). Thus, the response to tail illumination is not a simple reflex, but includes a behavioural choice. Reticulospinal neurones play a crucial role in the initiation of locomotion in lampreys. The response to unilateral tail illumination in rhombencephalic reticular cells was studied with extracellular single-unit recordings. It was found that neurones in the middle and posterior rhombencephalic reticular nuclei were activated bilaterally. Tonic activity or slow bursts (<0.5 Hz) were evoked, in some cases lasting up to 60 s after the stimulation. The response remained bilateral after transection of one lateral line nerve and the cerebellar commissure. Afferents from one side can thus activate reticulospinal cells on both sides through a pathway outside the cerebellar commissure. This bilateral activation of reticulospinal neurones is presumably responsible for the activation of spinal locomotor networks, without any directional bias to the left or the right side, and for the rectilinear swimming observed in behavioural experiments. In the caudal part of the termination area of the lateral line nerve afferents, neurones with contralateral projections were retrogradely stained with horseradish peroxidase. These neurones appear to be likely candidates for mediating the contralateral effects of the lateral line fibres.


Sensors ◽  
2021 ◽  
Vol 21 (12) ◽  
pp. 3980
Author(s):  
Dong Xu ◽  
Yuanlin Zhang ◽  
Jian Tian ◽  
Hongjie Fan ◽  
Yifan Xie ◽  
...  

The multi-sensor artificial lateral line system (ALLS) can identify the flow-field’s parameters to realize the closed-loop control of the underwater robotic fish. An inappropriate sensor placement of ALLS may result in inaccurate flow-field parametric identification. Therefore, this paper proposes a method to optimize the sensor placement configuration of the ALLS, which mainly included three algorithms, the feature importance algorithm based on mean and variance (MVF), the feature importance algorithm based on distance evaluation (DF), and the information redundancy (IR) algorithm. The optimal sensor placement performance selected by this method is verified by simulation. In addition, further experimental verification was conducted using the ALLS. Compared with the uniform sensor placement configuration mentioned in recent studies, the experimental results suggest that the optimal sensor placement method can achieve a more effective prediction of the flow-field parameters, therefore strengthening the underwater robotic fish’s perception and control function.


1934 ◽  
Vol 18 (1) ◽  
pp. 89-91 ◽  
Author(s):  
Hudson Hoagland

Records of spontaneous discharge of nerve impulses, similar to that previously described in catfish and in trout, have been obtained from lateral-line nerves of goldfish and perch, by the use of concentric micro electrodes slipped under the nerve in situ. These impulses have been followed into the central nervous system. They enter the tuberculum acusticum and thence apparently spread diffusely through the cerebellum. Cutting the lateral-line nerve on one side silences the ipsilateral tuberculum acusticum, but only reduces the intensity of ipsilateral cerebellar activity. Cutting the remaining lateral-line nerve silences activity throughout the tuberculum acusticum and the cerebellum. The maintenance of tonic activity in the tuberculum acusticum by way of lateral-line discharge may account for the inhibitory effects of the lateral-line system on auditory responses.


1933 ◽  
Vol 16 (4) ◽  
pp. 715-732 ◽  
Author(s):  
Hudson Hoagland

1. The lateral-line nerves of trout as well as those of catfish are found to discharge impulses spontaneously at a high frequency. 2. The frequency of nerve impulse discharge is measured as a function of the number of participating receptor groups (lateral-line sense organs). A quantitative analysis is made of the contribution to the total response made by each group of sense organs. 3. An analysis of the variability of the response is presented which makes it possible to estimate quantitatively the longitudinal extent of damage to the neuromasts due to surgical manipulation. 4. A method is described for recording the response of a single nerve fiber in the lateral-line trunk. 5. The frequency of the spontaneous discharge from the lateral-line nerve trunk when plotted as a function of temperature according to the Arrhenius equation yields a temperature characteristic of approximately 5000 calories. 6. The variability of the frequency of response as a function of temperature indicates the existence of temperature thresholds for the spontaneous activity of the neuromasts. 7. A possible basis for the spontaneous activity is considered. It is pointed out that the lateral-line system may serve as a model of the Purkinje cells of the cerebellum.


1983 ◽  
Vol 102 (1) ◽  
pp. 223-238 ◽  
Author(s):  
I. J. RUSSELL ◽  
D. A. LOWE

1. Microphonic and summating potentials were recorded extracellularly from lateral line organs in the suborbital canal of the perch in response to sinusoidal movements of canal fluid. 2. These potentials were changed in amplitude, shape and phase, relative to the mechanical stimulus, by electrical stimulation of efferent fibres in the lateral line nerve. 3. The receptor potential amplitude/stimulus intensity relationships for the microphonic and summating potentials saturated at high levels of stimulation, and at progressively lower amplitudes with increasing frequencies of mechanical stimulation. Efferent stimulation tended to reduce this rate of saturation. 4. Amplitude versus frequency relationships plotted at different stimulus intensities for the microphonic potential showed that the lateral line organs were most sensitive to frequencies between 35–65 Hz (centre frequency), and at these frequencies efferent stimulation caused the greatest increase in amplitude. 5. Analysis of the second order and third order harmonic components of the microphonic showed that these were reduced by efferent stimulation and that the strongest reduction occurred at the centre frequency. 6. The phase of the receptor potential led that of the mechanical stimulus at very low frequencies by nearly 90°. This changed to zero phase at the centre frequency and to a phase lag at higher frequencies. Efferent stimulation caused no change in phase of the microphonic relative to the control state at the centre frequency, but caused a progressive phase lead and lag as the frequency was decreased and increased respectively about the centre frequency. 7. In the linear response range, the lateral line organs responded as critically damped low frequency resonators to the velocity of the stimulus. Efferent stimulation appeared to alter the damping of this resonance. The possibility is discussed that efferent stimulation can alter the mechanical properties of the lateral line hair cells.


1998 ◽  
Vol 201 (1) ◽  
pp. 91-102 ◽  
Author(s):  
J C Montgomery ◽  
S Coombs

Video-tape recordings of prey-capture behaviour were made to demonstrate that stargazers can detect and capture prey in the dark and to determine the range of prey movement velocities that resulted in prey capture. Electrophysiological recording techniques were then used to determine how an artificial source (a sphere), moving at speeds within the range of recorded prey movement velocities, was encoded by anterior lateral line nerve fibres innervating the preopercular-mandibular canals on the head. A vibrating sphere was also used to measure frequency-response characteristics to determine the bandwidth of response and fibre origin (type of neuromast and location). In order to measure the relevant stimulus parameters likely to govern neural responses, the pressure-gradient pattern produced by the moving sphere was characterised with a pair of miniature hydrophones separated by approximately the same distance as head lateral line canal pores on stargazers. At least four different features of neural response patterns, including direction-dependent changes in the overall envelope of the firing rate pattern, could be predicted on the basis of measured pressure-gradient patterns. The dominant features of both the pressure-gradient and neural response patterns were produced by the wake behind the moving sphere, but behavioural observations indicated that stargazers were responding to the bow of an approaching prey, rather than its wake. Although the form of the wake behind the moving sphere is unlikely to be a good match for the stimulus mediating prey detection, these results clearly establish that pressure-gradient patterns are good predictors of neural response patterns. Thus, similar measurements of pressure-gradient patterns produced by more biologically relevant sources can be used to predict peripheral lateral line responses and stimulus features likely to be of key importance.


Author(s):  
Valentina Saccomanno ◽  
Heather M Love ◽  
Amy L Sylvester ◽  
Wen-Chang Li

Xenopus laevis has a lateral line mechanosensory system throughout its full life cycle and a previous study on pre-feeding stage tadpoles revealed that it may play a role in motor responses to both water suction and water jets. Here, we investigated the physiology of the anterior lateral line system in newly hatched tadpoles and the motor outputs induced by its activation in response to brief suction stimuli. High-speed videoing showed tadpoles tended to turn and swim away when strong suction was applied close to the head. The lateral line neuromasts were revealed by using DASPEI staining, and their inactivation with neomycin eliminated tadpole motor responses to suction. In immobilised preparations, suction or electrically stimulating the anterior lateral line nerve reliably initiated swimming but the motor nerve discharges implicating turning was observed only occasionally. The same stimulation applied during ongoing fictive swimming produced a halting response. The anterior lateral line nerve showed spontaneous afferent discharges at rest and increased activity during stimulation. Efferent activities were only recorded during tadpole fictive swimming and were largely synchronous with the ipsilateral motor nerve discharges. Finally, calcium imaging identified neurons with fluorescence increase time-locked with suction stimulation in the hindbrain and midbrain. A cluster of neurons at the entry point of the anterior lateral line nerve in the dorsolateral hindbrain had the shortest latency in their responses, supporting their potential sensory interneuron identity. Future studies need to reveal how the lateral line sensory information is processed by the central circuit to determine tadpole motor behaviour.


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