The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

The sensory basis of rheotaxis in the blind Mexican cave fish, Astyanax fasciatus

The sensory basis of rheotaxis (orientation to currents) was investigated in the blind Mexican cave fish, Astyanax fasciatus. An unconditioned rheotactic response to uniform velocity flows was exhibited, with a threshold of less than 3 cm s⁻¹. Disabling the entire lateral line or the superficial neuromast receptor class increased the rheotactic threshold to greater than 9 cm s⁻¹. A pharmacological block of the lateral line canal system alone had no effect. These results demonstrate that the superficial lateral line system controls rheotaxis at low current velocities. The effect of pairing an odor stimulant with the water current dropped the rheotactic threshold to less than 0.4 cm s⁻¹. This study provides a clear behavioral role for the superficial neuromasts where none previously existed, and also establishes a link between the mechanosensory lateral line and olfactory systems in the olfactory search behavior of the cave fish. Accepted: 9 January 1999     

Variations of glycogen: I. Following stimulation of Knollenorgan sensory cells,a lateral line electroreceptor of mormyrid fish

The metabolism of glycogen was studied in sensory cells of the mormyrid fish, Gnathonemus petersii. Knollenorgans, specific cutaneous electroreceptor organs of the lateral line system, have a spontancous electrical activity and their resting discharge in the absence of stimulation is about 0.04 kHz. Various types of stimulation can produce an increase in frequency; the highest frequency (1.30 kHz) is obtained by moving the Knollenorgan above water level. Glycogen was visualized in ultrathin sections after fixation in a solution of potassium ferricyanide and osmium tetroxide. The density of glycogen particles was determined morphometrically in sensory cells before stimulation, after high-frequency activity, and after reimmersion in water. An increase in the electrical activity of the Knollenorgan resulted in a decrease of the glycogen content of sensory cells. The glycogen store was replenished to about 85% of control within 40 min after stimulation and subsequent reimmersion. The results demonstrate that glycogen in the sensory cells of the Knollenorgan represents an energy source which can be catabolized during high electrical activity and replenished during rest.     

Coping with flow: behavior, neurophysiology and modeling of the fish lateral line system

With the mechanosensory lateral line fish perceive water motions relative to their body surface and local pressure gradients. The lateral line plays an important role in many fish behaviors including the detection and localization of dipole sources and the tracking of prey fish. The sensory units of the lateral line are the neuromasts which are distributed across the surface of the animal. Water motions are received and transduced into neuronal signals by the neuromasts. These signals are conveyed by afferent nerve fibers to the fish brain and processed by lateral line neurons in parts of the brainstem, cerebellum, midbrain, and forebrain. In the cerebellum, midbrain, and forebrain, lateral line information is integrated with sensory information from other modalities. The present review introduces the peripheral morphology of the lateral line, and describes our understanding of lateral line physiology and behavior. It focuses on recent studies that have investigated: how fish behave in unsteady flow; what kind of sensory information is provided by flow; and how fish use and process this information. Finally, it reports new theoretical and biomimetic approaches to understand lateral line function.     

The responses of central octavolateralis cells to moving sources

Mechanosensory lateral line units recorded from the medulla (medial octavolateralis nucleus) and midbrain (torus semicircularis) of the bottom dwelling catfish Ancistrus sp. responded to water movements caused by an object that passed the fish laterally. In terms of peak spike rate or total number of spikes elicited responses increased with object speed and sometimes showed saturation (Figs. 7, 14). At sequentially greater distances the responses of most medullary lateral line units decayed with object distance (Fig. 11). Units tuned to a certain object speed or distance were not found. The signed directionality index of most lateral line units was between –50 and +50, i.e. these units were not or only slightly sensitive to the direction of object motion (Figs. 10, 17). However, some units were highly directionally sensitive in that the main features of the response histograms and/or peak spike rates clearly depended on the direction of object movement (e.g. Fig. 9C, D and Fig. 16). Midbrain lateral line units of Ancistrus may receive input from more than one sensory modality. All bimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. Units which receive bimodal input may show an extended speed range (e.g. Fig. 18).Abbreviations MON medial octavolateralis nucleus - MSR mean spike rate - PSR peak spike rate - p-p peak-to-peak - SDI signed directionality index     

Behavioral and electrophysiological evidences that the lateral line is involved in the inter-sexual vibrational communication of the himé salmon (landlocked red salmon,Oncorhynchus nerka)

Characteristic vibrational signals are suggested to be exchanged between the sexes during the spawning behavior in the himé salmon (landlocked red salmon, Oncorhynchus nerka). To check whether the lateral line is used to detect and process these vibrational signals, we examined how Co²⁺, which is known to block the mechano-electrical transduction in the lateral line detector, affects both the spawning behavior and lateral line response of the male himé salmon. The results showed that Co²⁺ blocked both the spawning behavior towards the vibrating model (Fig. 2) and the lateral line response to the vibrational stimuli (Figs. 5, 6), if the fish were forced to swim in the water containing 1.0 mM Co²⁺ for 1 to 1.5 h or longer in the presence of 0.25 mM Ca²⁺. 0.1 mM Co²⁺ had similar but weaker effects. These results indicate that the vibrational signals from the vibrating model are detected and processed by the lateral line system to elicit the spawning behavior. These are the first experimental evidences that the lateral line sense is involved in the communicational behavior of the fish.     

Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates

The lateral line system of fishes and amphibians comprises two ancient sensory systems: mechanoreception and electroreception. Electroreception is found in all major vertebrate groups (i.e. jawless fishes, cartilaginous fishes, and bony fishes); however, it was lost in several groups including anuran amphibians (frogs) and amniotes (reptiles, birds, and mammals), as well as in the lineage leading to the neopterygian clade of bony fishes (bowfins, gars, and teleosts). Electroreception is mediated by modified “hair cells,” which are collected in ampullary organs that flank lines of mechanosensory hair cell containing neuromasts. In the axolotl (a urodele amphibian), grafting and ablation studies have shown a lateral line placode origin for both mechanosensory neuromasts and electrosensory ampullary organs (and the neurons that innervate them). However, little is known at the molecular level about the development of the amphibian lateral line system in general and electrosensory ampullary organs in particular. Previously, we identified Eya4 as a marker for lateral line (and otic) placodes, neuromasts, and ampullary organs in a shark (a cartilaginous fish) and a paddlefish (a basal ray‐finned fish). Here, we show that Eya4 is similarly expressed during otic and lateral line placode development in the axolotl (a representative of the lobe‐finned fish clade). Furthermore, Eya4 expression is specifically restricted to hair cells in both neuromasts and ampullary organs, as identified by coexpression with the calcium‐buffering protein Parvalbumin3. As well as identifying new molecular markers for amphibian mechanosensory and electrosensory hair cells, these data demonstrate that Eya4 is a conserved marker for lateral line placodes and their derivatives in all jawed vertebrates.     

Studies on the effects of Ca2++ and Co++ on the swimming behavior of the blind Mexican cave fish

Summary The hypothesis that the blind cave fish (Astyanax hubbsi) adjusts the level of stimulation to its lateral line system (LLS) by varying its own velocity was examined. When the sensitivity of the LLS sense organs was reduced by lowering the Ca²⁺ concentration in the water or by adding Co²⁺ the fish compensated for this by swimming at a higher velocity.Abbreviation LLS lateral line system     

Lateral line pore diameters correlate with the development of gas bubble trauma signs in several Columbia River fishes

Gas bubble trauma (GBT) caused by gas supersaturation of river water continues to be a problem in the Columbia River Basin. A common indicator of GBT is the percent of the lateral line occluded with gas bubbles; however, this effect has never been examined in relation to lateral line morphology. The effects of 115, 125 and 130% total dissolved gas levels were evaluated on five fish species common to the upper Columbia River. Trunk lateral line pore diameters differed significantly (P<0.0001) among species (longnose sucker>largescale sucker>northern pikeminnow>/=chinook salmon>/=redside shiner). At all supersaturation levels evaluated, percent of lateral line occlusion exhibited an inverse correlation to pore size but was not generally related to total dissolved gas level or time of exposure. This study suggests that the differences in lateral line pore diameters between species should be considered when using lateral line occlusion as an indicator of gas bubble trauma.     

Ultrastructure of free neuromasts of Bathygobius fuscus (gobiidae) and canal neuromasts of Apogon cyanosoma (apogonidae)

Light and electron microscopic observations were made on the lateral line organs of the free neuromasts of the goby Bathygobius fuscus and the canal neuromasts of the cardinal fish Apogon cyanosoma. As in other lateral line systems, each neuromast consists of hair cells, supporting cells and mantle supporting cells, the whole being covered by a cupula. In B. fuscus the free neuromasts are mounted on papillae and have hair cells with stereocilia up to 2.5 μm long and a single kinocilium at least 25 μm long. Each neuromast is covered by a vane-like cupula that can be divided into two regions. The central region over the sensory area contains columns of myelin-like figures. These figures are absent from the outer region covering the mantle. The canal neuromasts of A. cyanosoma are diamond-shaped with up to 1,500 hair cells. The cupula is unusual in having a channel that lies over the sensory region. The hair cells have up to 45 stereocilia, the tallest reaching 2.5 μm, and a kinocilium at least 5 μm long. Tip links are shown for the first time between rows of stereocilia of the hair cells of lateral line neuromasts. The presence of tip links has now been demonstrated for all acousticolateral hair cell systems.     

The oscar, <Emphasis Type="Italic">Astronotus ocellatus</Emphasis>, detects and discriminates dipole stimuli with the lateral line system

We studied the role of the lateral line system for detection and discrimination of dipole stimuli in the oscar, Astronotus ocellatus (Family Cichlidae), and determined detection thresholds in still water and frequency discrimination capabilities in still and turbulent water. Average detection threshold of six animals for a 100-Hz dipole stimulus was 0.0059 μm peak-to-peak water displacement at the surface of the fish. After inactivation of the neuromast receptor organs of the lateral line system with the antibiotic streptomycin, dipole detection was reduced, but recovered within 2–4 weeks. This suggests that the oscar relied strongly on hydrodynamic information received by the lateral line system. Five oscars learned to discriminate a 100-Hz stimulus from 70 Hz and lower frequencies. When turbulence was introduced into the experimental tank, fish were still able to discriminate 100 Hz from frequencies 70 Hz and lower indicating that frequency discrimination mediated by the lateral line system was not reduced in turbulent water.     

A lateral line analogue in cephalopods: water waves generate microphonic potentials in the epidermal head lines ofSepia andLolliguncula

Summary Many cephalopods have lines of ciliated cells on their head and arms. In the cuttlefishSepia and the squidLolliguncula, electrophysiological recordings clearly identify these epidermal lines as an invertebrate analogue to the mechanoreceptive lateral lines of fish and aquatic amphibians and thus as another example of convergent evolution between a sophisticated cephalopod and vertebrate sensory system. Stimulation of the epidermal lines with local water displacements, generated by a vibrating sphere, causes receptor potentials that have many features known from lateral line microphonic potentials. The minimal threshold of the head lines is 0.2 m peak-to-peak water displacement (calculated at the skin surface) at 75–100 Hz.     

Responses to dipole stimuli of anterior lateral line nerve fibres in goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>, under still and running water conditions

We investigated how fibres in the anterior lateral line nerve of goldfish, Carassius auratus, respond to sinusoidal water motions in a background of still or running water. Two types of fibres were distinguished: type I fibres, which most likely innervate superficial neuromasts, were stimulated by running water (10 cm s⁻¹) while type II fibres, which most likely innervate canal neuromasts, were not stimulated by running water. The responses of type I fibres to sinusoidal water motions were masked in running water whereas responses of type II fibres were not masked. These findings are in agreement with previous data obtained from the posterior lateral line nerve of goldfish. Furthermore, we demonstrate here that for type I fibres the degree of response masking increased with increasing flow velocity. Finally, the ratio between responses that were masked in running water (type I) and those that were not masked (type II) increases with increasing flow velocity. Flow fluctuations that were generated by a cylinder in front of the fish did not affect ongoing activity in the flow, nor the dipole-evoked responses. The findings are discussed with respect to particle image velocimetry data of the water motions generated in the experiments.     

Kármán vortex street detection by the lateral line

Fish use the lateral line system for prey detection, predator avoidance, schooling behavior, intraspecific communication and spatial orientation. In addition the lateral line may be important for station holding and for the detection of the hydrodynamic trails (vortex streets) generated by swimming fish. We investigated the responses of anterior lateral line nerve fibers of goldfish, Carassius auratus, to unidirectional water flow (10 cm s⁻¹) and to running water that contained a Kármán vortex street. Compared to still water conditions, both unidirectional water flow and Kármán vortex streets caused a similar increase in the discharge rate of anterior lateral line nerve fibers. If exposed to a Kármán vortex street, the amplitude of spike train frequency spectra increased at the vortex shedding frequency. This increase was especially pronounced if the fish intercepted the edge of a Kármán vortex street. Our data show that the vortex shedding frequency can be retrieved from the responses of anterior lateral line nerve fibers.     

A new electroreceptive teleost:Xenomystus nigri (Osteoglossiformes: Notopteridae)

Summary The African knife fish,Xenomystus nigri, is found to be sensitive to weak electric fields by the method of averaged evoked potentials from the brain. Slow waves and spikes were recorded in or near the lateral line area of the medulla and the torus semicircularis of the mesencephalon in response to long pulses (best > 50 ms) and low frequency sine waves (best ca. 10 Hz) of voltage gradients down to < 10 V/cm. Evoked waves in the lateral line area are a sequence of negative and positive deflections beginning with a first peak at ca. 24 ms; in the torus semicircularis the first peak is at ca. 37 ms. Spikes are most likely in the torus between 50 and 80 ms after ON. At each recording locus there is a best axis of the homogeneous electric field and a better polarity. Effects of stimulus intensity, duration and repetition are described. The physiological properties are similar to those of ampullary receptor systems in mormyriforms, gymnotiforms and siluriforms.Confirming Braford (1982),Xenomystus has a large medullary nucleus resembling the nucleus otherwise peculiar to mormyriforms, gymnotiforms and siluriforms and now called the electrosensory lateral line lobe (ELLL; formerly the posterior lateral line lobe). We describe the projections of anterior and posterior lateral line nerves by HRP applied to the proximal stump of a cut nerve. A descending central ramus of the anterior lateral line nerve and a lateral component of the ascending ramus of the posterior lateral line nerve end in part in the ELLL.Electroreception, including the system of discrete central structures mediating it, is for the first time found to be less than an ordinal or even a family character, but apparently a characteristic of the subfamily Xenomystinae. Species of the other subfamily, Notopterinae as well as of the other families of osteoglossiforms (Osteoglossidae, Hiodontidae and Pantodontidae), lack the ELLL.Notopterus andPantodon are found to lack the evoked potential.The positive finding of evoked activity to feeble electric field is found to be the most practical method for searching widely among fishes for the presence of the electrosense modality and its central pathways. The anatomical criterion of an ELLL can now be taken to be a good criterion for the presence of this sensory system. The absence of evoked response correlates well with the absence of an ELLL.Abbreviations ELLL electrosensory lateral line lobe - HRP horseradish peroxidase - TS torus semicircularis     

Responses of the goldfish head lateral line to moving objects

We investigated how fibers in the anterior lateral line nerve of goldfish, Carassius auratus, respond to water motions generated by an object that was moved alongside the fish. Motion direction was from anterior to posterior or opposite, object diameter was between 0.1 and 4 cm and the distance between object and fish varied between 1 and 6 cm. Fibers exhibited monophasic responses characterized by a transient increase in discharge rate, biphasic responses consisting of an increase followed by a decrease in discharge rate or vice versa, or triphasic responses characterized by a rate increase followed by a decrease and again an increase or by the inverse pattern. In two-thirds of the fibers response patterns depended on object motion direction. Of these, about 60% responded to a reversal of motion direction with an inversion of the response pattern. Our results differ from previous data obtained from posterior lateral line nerve fibers in the relative proportions of the observed response patterns, and by a much smaller proportion of fibers that exhibited a direction-dependent response. These differences can be explained by the fact that the spatial orientations of the neuromasts on the head are more heterogenuous than on the trunk.     

Central Nervous System Changes Related to the Reduction of Visual Input in a Naturally Blind Fish (Astyanax hubbsi)

Tectal anatomy and physiology of the blind cave characin, Astyanaxhubbsi, have been compared with that of its sighted ancestorAstyanax mexicanus (the river fish) and with goldfish. Normaland experimental neuroanatomic methods have revealed that, withthe exception of a greatly reduced retinotectal projection,connectivity and structure of cave fish tecta are similar tothose described in sighted species. It appears that the rudimentaryretinotectal input is nonfunctional, since no tectal evokedresponses could be elicited with electrical or visual stimulationof the optic cyst, and all attempts to visually condition cavefish were unsuccessful. Attempts have also been made to record somatosensory, auditoryand lateral line activity in the tecta of the blind and sightedfish. A sparse somatic representation was found in the deeperportion of the sighted fish tecta which contrasts with a dense,well-organized one in the cave fish. No tectal responses werefound to auditory or lateral line stimuli. CNS plasticity is discussed in relation to studies of fish,amphibians, reptiles, birds and mammals, in which a reductionof sensory input by any one of a number of means has resultedin alterations of structure and function.     

Activity of lateral line efferents in the axolotl (Ambystoma mexicanum)

Summary Activity of efferent fibers was recorded from the ramus ophthalmicus superficialis of the head lateral line nerve and the ramus medialis of the trunk lateral line nerve of the axolotl Ambystoma mexicanum. Baseline activity and activity evoked by sensory stimuli were examined. Electrical stimulation of selected branches was used to determine the conduction velocity and the branching pattern of efferent fibers. The influence of lesions at different levels in the CNS on efferent activity was studied.Up to 5 units with baseline activity were found in a single ramus of the lateral line nerve. Discharge rates were variable and highly irregular; they differed between units of the same branch. Bursting activity occurred in 62% of the units. Movements of the animal were accompanied by activity in up to 8 efferent units in a single nerve.Efferent activity could be elicited or modified by stimulation of visual, labyrinthine, somatosensory, and lateral line systems. Stimulation of the electrosensory system had no effect. Individual efferent neurons innervated different fields in the lateral line periphery. Conduction velocities of efferent fibers ranged from 5 to 12 m/s.Efferent units received input from various sources at different brain levels up to the diencephalon. These in puts determined the baseline activity. The mechanosensory input was mediated at the medullary level.Abbreviations r.m. ramus medialis - r.o.s. ramus ophthalmicus superficialis - r.s. ramus superior     

Sensory development of the Antarctic silverfish Pleuragramma antarcticum: a test for the ontogenetic shift hypothesis

In 1996 Montgomery proposed an ontogenetic shift in the use of visual and non-visual senses in Antarctic notothenioid fishes, with visual dominance in larval fishes giving way to non-visual senses in adults. One prediction of the hypothesis is timing differences in the development of the respective sensory systems, with the visual system expected to develop earlier than the other systems. The volume of certain brain centres can be determined from fixed material and should correlate with sensory development. This study determined the relative volumes of visual and lateral line brain areas, and relative eye size as a function of fish length in Pleuragramma antarcticum.The relative volume of optic tectum was largest in larval fish, exhibiting a negative allometry with growth. The eminentia granularis, and crista cerebellaris (lateral line associated areas) were not recognisable in the smallest larvae; they became differentiated at standard lengths of 10–20 mm and their relative volumes continued to increase over the size range of fish studied (up to 150 mm standard length). Relative eye diameter decreased dramatically over the size range 5–25 mm and then increased such that relative eye diameter doubled over the size range 25–30 mm. A similar, but less extreme, pattern was seen over the size range 30–60 mm. Above 60 mm relative eye diameter increased slightly with size. Our interpretation is that eye growth and somatic growth are on separate trajectories, and the breaks in the relative eye diameter curve result from overwinter periods when somatic growth is static, but the eye continues to grow. These results provide support for the ontogenetic shift hypothesis, and indicate that the timing of the shift probably occurs after the second winter. Received: 22 October 1996 / Accepted: 10 January 1997