scholarly journals Initiation of locomotion by lateral line photoreceptors in lamprey: behavioural and neurophysiological studies

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.

2014 ◽  
Vol 112 (6) ◽  
pp. 1329-1339 ◽  
Author(s):  
Melanie Haehnel-Taguchi ◽  
Otar Akanyeti ◽  
James C. Liao

The lateral line system of fishes contains mechanosensory receptors along the body surface called neuromasts, which can detect water motion relative to the body. The ability to sense flow informs many behaviors, such as schooling, predator avoidance, and rheotaxis. Here, we developed a new approach to stimulate individual neuromasts while either recording primary sensory afferent neuron activity or swimming motoneuron activity in larval zebrafish ( Danio rerio). Our results allowed us to characterize the transfer functions between a controlled lateral line stimulus, its representation by primary sensory neurons, and its subsequent behavioral output. When we deflected the cupula of a neuromast with a ramp command, we found that the connected afferent neuron exhibited an adapting response which was proportional in strength to deflection velocity. The maximum spike rate of afferent neurons increased sigmoidally with deflection velocity, with a linear range between 0.1 and 1.0 μm/ms. However, spike rate did not change when the cupula was deflected below 8 μm, regardless of deflection velocity. Our findings also reveal an unexpected sensitivity in the larval lateral line system: stimulation of a single neuromast could elicit a swimming response which increased in reliability with increasing deflection velocities. At high deflection velocities, we observed that lateral line evoked swimming has intermediate values of burst frequency and duty cycle that fall between electrically evoked and spontaneous swimming. An understanding of the sensory capabilities of a single neuromast will help to build a better picture of how stimuli are encoded at the systems level and ultimately translated into behavior.


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.


Author(s):  
Jennifer D. Liddicoat ◽  
B. L. Roberts

The sense organs of the lateral-line system of lower aquatic vertebrates are mechanoreceptors which respond to water movements. They are distributed over the body, usually in lines which form a definite pattern on the head and along each side of the trunk. In the Cyclostomes the sense organs project from the body surface ('free neuromasts'); in other aquatic vertebrates they are usually housed in canals which are sunk into the dermis and which open at regular intervals to the exterior, although in some teleosts and in all modern amphibia the canal system has been secondarily lost and the neuromasts are once again situated externally.


2010 ◽  
Vol 6 (3) ◽  
pp. 402-405 ◽  
Author(s):  
James C. Liao

The lateral line system of larval zebrafish can translate hydrodynamic signals from the environment to guide body movements. Here, I demonstrate a spatial relationship between the organization of afferent neurons in the lateral line ganglion and the innervation of neuromasts along the body. I developed a whole cell patch clamp recording technique to show that afferents innervate multiple direction-sensitive neuromasts, which are sensitive to low fluid velocities. This work lays the foundation to integrate sensory neuroscience and the hydrodynamics of locomotion in a model genetic system.


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.


1994 ◽  
Vol 197 (1) ◽  
pp. 399-403
Author(s):  
Y Mukai ◽  
H Yoshikawa ◽  
H Kobayashi

Free mechanosensory neuromasts of larval fishes have been described as playing a complementary role to vision in feeding behaviour (Disler, 1971; Iwai, 1972a,b). In certain species or under limited conditions, free neuromasts play a major role in detecting prey. The larvae of mottled sculpin Cottus bairdi can feed on Artemia in the dark by using free neuromasts (Jones and Janssen, 1992). Artificially blinded surface-feeding Aplocheilus lineatus can detect insects on the water surface by means of free neuromasts (Muller and Schwarts, 1982; Tittel et al. 1984; Bleckmann, 1988; Bleckmann et al. 1989). Furthermore, vibrations produced by swimming crustaceans are known to be a potent natural stimulus for the lateral line system in the Antarctic fish Pagothenia borchgrevinki (Montgomery and Macdonald, 1987; Montgomery, 1989). We found that larvae of a plankton feeder, the willow shiner Gnathopogon elongatus caerulescens (Sauvage) (Cypriniformes, Cyprinidae), fed on nauplii of Artemia in complete darkness. Ototoxic compounds, such as streptomycin, have been shown to disturb the function of the lateral line organ or free neuromasts (Kaus, 1987; Blaxter and Fuiman, 1989; Janssen, 1990; Jones and Janssen, 1992). Willow shiner larvae treated with streptomycin sulphate no longer feed on Artemia in the dark (Y. Mukai, in preparation). The willow shiner inhabits calm lakes and feeds on zooplanktonic prey (Nakamura, 1949). The larvae show a high sensitivity to minute water displacements. From these observations and from our findings, it appears that larval willow shiner must feed on zooplankton by using free neuromasts in the dark. In larval willow shiner, the vane-like cupulae of the free neuromasts protrude from the body surface and the long cupulae are 100-250 microm in length (Mukai and Kobayashi, 1991). The prey is detected by the free neuromasts as a result of a slight bending of the cupula in response to local water movements. The shape of the cupula, especially its length, must therefore be related to the sensitivity of the free neuromast, as inferred from the results of Coombs and Janssen (1989) and van Netten and Kroese (1989).


1984 ◽  
Vol 108 (1) ◽  
pp. 315-328 ◽  
Author(s):  
PETER GÖRNER ◽  
PETER MOLLER ◽  
WOLFGANG WEBER

1. Intact Xenopus sp. responded to a train of surface waves with a single, stimulus-directed motor response which consisted of a turning component and a displacement component. The turning angle increased in a linear fashion with the stimulus angle. 2. The magnitude of the turning angle was not affected by (a) the size of the animal, (b) the way the surface wave was elicited (with a drop of water or by dipping a rod into the water), (c) reflected waves and (d) the number of successively administered stimuli. 3. With no lateral-line organs left intact Xenopus could still localize the origin of a surface wave, but with reduced accuracy. 4. With only two stitches left intact on the left and on the right occipital lines, the turning angles were more widely scattered for stimuli placed at angles larger than 90°. The scatter was even larger than that of the equivalent responses from animals without a functional lateral-line system, i.e. the directional responsiveness in the partly lesioned animals was less accurate than in those with their entire lateral-line inoperative. 5. Xenopus with four or two ipsilateral occipital stitches left intact were no longer able to orientate accurately. When the animal was stimulated on the lesioned side it frequently turned to the wrong side. These errors were absent or less frequent when the animal was stimulated on the intact side. 6. The lesion experiments indicated that (a) a few organs provide sufficient information for an appropriate turning response, but the turnings were only roughly directed towards the stimulus, and (b) the decision whether Xenopus localizes a stimulus on the left or right side depends on whether the central nervous system receives information from one or both sides.


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.


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