Lateral line

Sensory system in fish

Oblique view of a goldfish

(Carassius auratus), showing pored scales of the lateral line system

The lateral line, also called the lateral line organ (LLO), is a system of

schooling

behavior, predation, and orientation.

Early in the evolution of fish, some of the receptive organs of the lateral line were modified to function as the

electroreceptors called ampullae of Lorenzini

.

Function

The lateral line system allows the detection of movement, vibration, and pressure gradients in the water surrounding an animal, providing spatial awareness and the ability to navigate in the environment. This plays an essential role in orientation, predation, and

fish schooling.^[1] Analysis has shown that the lateral line system should be an effective passive sensing system able to discriminate between submerged obstacles by their shape.^[2][3]

The lateral line system enables predatory fishes to detect vibrations made by their prey, and to orient towards the source to begin predatory action.[4] Blinded predatory fishes remain able to hunt, but not when lateral line function is inhibited by cobalt ions.^[5]

The lateral line plays a role in fish schooling. Blinded Pollachius virens were able to integrate into a school, whereas fish with severed lateral lines could not.^[6] It may have evolved further to allow fish to forage in dark caves. In Mexican blind cave fish, Astyanax mexicanus, neuromasts in and around the orbit of the eye are bigger and around twice as sensitive as those of surface-living fish.^[7]

One function of schooling among prey fish may be to confuse the lateral line of predatory fishes. A single prey fish creates a rather simple particle velocity pattern, whereas the pressure gradients of many closely swimming (schooling) prey fish overlap, creating a complex pattern. This makes it difficult for predatory fishes to identify individual prey through lateral line perception.^[8]

Anatomy

The lateral line system consists of canals that run along a fish's body, connecting rows of openings through the skin and scales to the water outside the body. Small sense organs, neuromasts, are positioned both at intervals along the canals, and on the surface of the body.

three-spined stickleback

with stained neuromasts

Lateral lines are usually visible as faint lines of pores running lengthwise down each side of a fish's body.

microvilli "hairs" which function as the mechanoreceptors.^[10] These bundles are organized in rough "staircases" of hairs of increasing length order.^[11]

Signal transduction

Lateral line rate coding indicates direction and sometimes strength of stimulus.

The hair cells are stimulated by the deflection of their hair bundles in the direction of the tallest "hairs" or stereocilia. The deflection allows cations to enter through a mechanically gated channel, causing depolarization of the hair cell. This depolarization opens Ca_v1.3 calcium channels in the basolateral membrane.^[12]

rate coding to transmit the directionality of a stimulus. The hair cells produce a constant, tonic rate of firing. As mechanical motion is transmitted through water to the neuromast, the cupula bends and is displaced according to the strength of the stimulus. This results in a shift in the cell's ionic permeability. Deflection towards the longest hair results in depolarization of the hair cell, increased neurotransmitter release at the excitatory afferent synapse, and a higher rate of signal transduction. Deflection towards the shorter hair has the opposite effect, hyperpolarizing the hair cell and producing a decreased rate of neurotransmitter release. These electrical impulses are then transmitted along afferent lateral neurons to the brain.^[10]

While both varieties of neuromasts utilize this method of transduction, their specialized organization gives them different mechanoreceptive capacities. Superficial organs are exposed more directly to the external environment. The organization of the bundles within their organs is seemingly haphazard, incorporating various shapes and sizes of

microvilli within bundles. This suggests coarse but wide-ranging detection.^[11] In contrast, the structure of canal organs allow canal neuromasts more sophisticated mechanoreception, such as of pressure differentials. As current moves across the pores of a canal, a pressure differential is created over the pores. As pressure on one pore exceeds that of another pore, the differential pushes down on the canal and causes flow in the canal fluid. This moves the cupula of the hair cells in the canal, resulting in a directional deflection of the hairs corresponding to the direction of the flow.^[13]

Electrophysiology

The mechanoreceptive hair cells of the lateral line structure are integrated into more complex circuits through their afferent and efferent connections. The synapses that directly participate in the transduction of mechanical information are excitatory afferent connections that utilize

glutamate.^[14] Species vary in their neuromast and afferent connections, providing differing mechanoreceptive properties. For instance, the superficial neuromasts of the midshipman fish, Porichthys notatus, are sensitive to specific stimulation frequencies.^[15] One variety is attuned to collect information about acceleration, at stimulation frequencies between 30 and 200 Hz. The other type obtains information about velocity, and is most receptive to stimulation below 30 Hz.^[15]

The motion detection system in fish works despite "noise" created by the fish itself. The brain copies the efferent commands it gives to the swimming muscles to the lateral line, effectively suppressing swimming noise and revealing small signals from the environment, such as from prey.^[16]

The efferent synapses to hair cells are inhibitory and use

corollary discharge system designed to limit self-generated interference. When a fish moves, it creates disturbances in the water that could be detected by the lateral line system, potentially interfering with the detection of other biologically relevant signals. To prevent this, an efferent signal is sent to the hair cell upon motor action, resulting in inhibition which counteracts the excitation resulting from reception of the self-generated stimulation. This allows the fish to retain perception of motion stimuli without interference created by its own movements.^[16]

Signals from the hair cells are transmitted along lateral neurons to the brain. The area where these signals most often terminate is the medial octavolateralis nucleus (MON), which probably processes and integrates mechanoreceptive information.[17] The deep MON contains distinct layers of basilar and non-basilar crest cells, suggesting computational pathways analogous to the electrosensory lateral line lobe of electric fish. The MON is likely involved in the integration of excitatory and inhibitory parallel circuits to interpret mechanoreceptive information.^[18]

Evolution

electroreceptive organs called ampullae of Lorenzini (red dots), illustrated here on the head of a shark, evolved from the mechanosensory lateral line organs (gray lines) of the last common ancestor of vertebrates.^[19][20]

The use of mechanosensitive hairs is homologous to the functioning of hair cells in the auditory and vestibular systems, indicating a close link between these systems.^[10] Due to many overlapping functions and their great similarity in ultrastructure and development, the lateral line system and the inner ear of fish are often grouped together as the octavolateralis system (OLS).^[21] Here, the lateral line system detects particle velocities and accelerations with frequencies below 100 Hz. These low frequencies create large wavelengths, which create strong particle accelerations in the near field of swimming fish that do not radiate into the far field as acoustic waves due to an acoustic short circuit. The auditory system detects pressure fluctuations with frequencies above 100 Hz that propagate to the far field as waves.^[22]

The electroreceptive organs called ampullae of Lorenzini, appearing as pits in the skin of sharks and some other fishes, evolved from the lateral line organ. It is basal to the jawed fishes.^[19] Passive electroreception using ampullae is an ancestral trait in the vertebrates, meaning that it was present in their last common ancestor.^[20]

The lateral line system is ancient and basal to the vertebrate clade; it is found in groups of fishes that diverged over 400 million years ago, including the lampreys, cartilaginous fishes, and bony fishes.^[23][24] Most amphibian larvae and some fully aquatic adult amphibians possess mechanosensitive systems comparable to the lateral line.^[25] The terrestrial tetrapods have secondarily lost their lateral line organs, which are ineffective when not submerged.^[24]

Vertebrates	Lampreys >440 mya Jawed fishes 430 mya Bony fishes Lobe-finned fishes Amphibians (as larvae; some as adults) Other tetrapods (no lateral line) Ray-finned fishes 425 mya Ampullae of Lorenzini
Lateral line

References

Further reading

• Coombs, S.; van Netten, S. (2006). "The Hydrodynamics and Structural Mechanics of the Lateral Line System". In R. E. Shadwick; G. V. Lauder (eds.). Fish Physiology: Fish Biomechanics. Academic Press. pp. 103–140.
  ISBN 978-0-0804-7776-3
  .
• Popper, A. N.; Platt, C. (1993). "Inner ear and lateral line of bony fishes". In Evans, D. H. (ed.). The Physiology of Fishes (1st ed.). CRC Press. pp. 99–136.
  ISBN 978-0-8493-8042-6
  .
• Schellart, Nico A. M.; Wubbels, René J. (1998). "The Auditory and Mechanosensory Lateral Line System". In Evans, David Hudson (ed.). The Physiology of Fishes (2nd ed.). CRC Press. pp. 283–312.
  ISBN 978-0-8493-8427-1
  .

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See also

• Artificial lateral line