Mauthner cell
Encyclopedia
The Mauthner Cells are a pair of big and easily identifiable neuron
s (one for each half of the body) located in the rhombomere
4 of the hindbrain in fish and amphibian
s that are responsible for a very fast escape reflex
(in the majority of animals - a so called C-start response). The cells are also notable for their unusual use of both chemical and electrical
synapses.
and lancelet
s), and are present in virtually all teleost fish, as well as in amphibians (including postmetamorphic
anurans). Some fish, such as the lumpsuckers seem to have lost the Mauthner cells however.
that is employed by fish and amphibian
s (including larval
anurans). There are two sequential stages in the C-start: first, the head rotates about the center of mass
towards the direction of future escape, and the body of the animal exhibits a curvature that resembles a letter C; then, at the second stage, the animal is propelled forward. The duration of these stages varies from species to species from about 10 to 20 ms for the first stage, and from 20 to 30 ms for the second. In fish this forward propulsion does not require contraction of the antagonistic muscle
, but results from the body stiffness and the hydrodynamic resistance of the tail
. When an antagonistic muscular contraction does occur during stage 2, the fish rotates in the opposite direction, producing a counter-turn, and a directional change.
, tactile or visual stimulus elicits a single action potential
in one M-cell, it always correlates with a contralateral C-start escape. An extremely quick mutual feedback
inhibitory circuit then assures that 1) only one M-cell reaches spiking threshold, as the C-start has to be unilateral by definition, 2) that only one action potential is fired.
The Mauthner cell-mediated C-start reflex is very quick, with about 5-10 ms latency between the acoustic/tactile stimulus
and the Mauthner cell discharge, and only about 2 ms between the discharge and the unilateral muscle contraction. Mauthner cells is thus the quickest motor neuron to respond to the stimulus. It makes the C-start response behaviorally important as a way to initiate the escape reflex in an all or nothing fashion, while the direction and speed of the escape can be corrected later through the activity of smaller motor neurons.
In larval
zebrafish about ~60% of the total population of reticulospinal neurons are also activated by a stimulus that elicits the M-spike and C-start escape. A well-studied group of these reticulospinal neurons are the bilaterally paired M-cell homologues denoted MiD2cm and MiD3cm. These neurons exhibit morphological similarities to the M-cell including a lateral and ventral dendrite. They are located in rhombomere
s 5 and 6 of hindbrain respectively, and also receive auditory input in parallel with the M-cell from the pVIIIth nerve. In fish, water jet stimuli that activate these neurons elicit non-mauthner initiated C-starts of a longer latency, compared with M-cell associated ones.
Although the M-cell is often considered the prototype of a command neuron
in vertebrate
s, this designation may not be fully warranted. Although electrical stimulation of the M-cell is sufficient for eliciting a C-start, this C-start is normally weaker than the one evoked by a sensory stimulus. Moreover, the C-start can be evoked even with the M-cell ablated
, although in this case the latency of the response increases. The most widely accepted model of the M-cell system, or brainstem escape network, is that the M-cell initiates a fixed action pattern to the left or right by activating a spinal motor circuit initially described by J. Diamond and colleagues, but the precise trajectory of the escape is encoded by population activity in the other classes of reticulospinal neurons functioning in parallel to the M-cell. This notion is supported by studies using in vivo calcium imaging in larval zebrafish which show that MiD2cm and MiD3cm are activated along with the M-cell when an offending stimulus is directed towards the head but not the tail, and are correlated with C-starts of a larger initial turn angle.
Another component of the escape response is mediated by cranial relay neurons that are activated by the Mauthner cell spike. These neurons are electrically coupled with motoneurons which innervate extraocular, jaw and opercular muscles and mediate pectoral fin adduction in hatchetfish
. This component of the neural circuit was first described by Michael V.L. Bennett and colleagues.
Mauthner cells are activated during prey capture near the surface of the water, as this type of hunting is dangerous for the fish, and it would benefit from leaving the surface as soon as possible after the prey is captured.
In adult postmetamorphic
anurans that do not have a tail, M-cells are nevertheless preserved and their discharges are associated with rapid movement of leg
s during an escape.
s which receive segregated inputs from various parts of the neural system. One dendrite projects laterally and the other projects either in the ventral or medial direction, depending on the species.
The ventral dendrite receives information from the optic tectum and spinal cord
while the lateral dendrite receives inputs from the octovolateralis systems (the lateral line
, accoustic inputs from the inner ear
, and inertial information from the statoliths brought by the cranial nerve VIII).
The fibers from the ipsilateral cranial nerve VIII terminate in excitatory mixed electrical
and glutamatergic synapses on the M-cell. They also electrically activate glycine
rgic inhibitory interneurons that terminate on the M-cells. Despite the inhibitory input having one more synapse in its pathway, there is no delay between the excitation and inhibition because the intervening synapse is electrical. It was shown that for weak stimuli the inhibition wins over the excitation, preventing the M-cell from a discharge, while for stronger stimuli excitation becomes dominant. The Inner ear
afferents also terminate with electrical synapses on a population PHP inhibitory interneurons (see below) to provide an additional level of feed forward inhibition. The Mauthner cell also has GABA
-, dopamine
-, serotonin
- and somatostatin
ergic inputs, each restricted to certain dendritic region.
Inputs from the optic tectum and the lateral line help control which way the C-startle bends by biasing the mauthner cells when there are obstacles in the vicinity. In cases where movement away from the stimulus is blocked, the fish way bend towards the disturbance.
is surrounded by a dense formation of neuropil, called the Axon cap. The high resistance of this axon cap contributes to the typical shape of the Mauthner cell field potential (see below). It its most advanced form the axon cap consists of a core, immediately adjacent to the Mauthner cell axon, and containing a network of very thin unmyelinated
fibers, and a peripheral part. This peripheral part contains the large unmyelinated fibers of the PHP neurons (see below) that mediate the inhibitory feedback to the Mauthner cell; the Mauthner cell itself also sends small dendrites from its axon hill to the peripheral part of the axon cap. Finally, the surface of the axon cap is covered with a cap wall composed of several layers of astrocyte
-like glial cells. Both glial cells and the unmyelinated fibers are coupled with each other by means of gap junction
s.
Evolutionary the axon cap is a more recent development than the Mauthner cell itself, so some animals, such as lamprey
s and eel
s, while having functional Mauthner cells, don't have axon cap at all, while some other animals, such as amphibia and lungfish
, do have a very simplified version of it.
network, which assures that a) only one of the two Mauthner cells fires in response to the stimulus; b) the Mauthner cell that fires, does it only once. Both these requirements are quite natural considering that the consequences of a single Mauthner cell discharge are so strong; a failure to comply with these two rules would not only prevent the animal from escaping, but could even physically damage it. The fastest part of this negative feedback network, which is also the one closest to the Mauthner cell, is that of the so called passive hyperpolarizing field potential or PHP neurons. The fibers of these neurons are located in the axon cap, and they receive inputs from both ipsilateral and contralateral Mauthner cells. The field potentials of PHP neurons are strongly positive, and form a part of the 'Signature field potential' of the Mauthner cell (see below), with the early (ipsilaterally initiated) component being called the Extracellular Hyperpolarizing Potential (EHP), and the later (contralaterally initiated) component being sometimes addressed in the literature as the Late Collateral Inhibition (LCI). The action of PHP neurons onto the Mauthner cells is mediated by electrical, and not chemical effects: the outward currents generated by the action potential
s in axon cap fibers flow inward across the Mauthner cell axon hillock
and hyperpolarize it.
of the Mauthner cell reaches from the cell to the midline of the hindbrain, promptly crosses it to the contralateral side, and then descends caudally along the spinal cord
. A single discharge of the M-cell achieves a whole set of parallel effects onto the spinal motor networks: 1) it monosynaptically excites large primary motoneurons at one side of the body; 2) disinaptically excites smaller motoneurons at the same side of the body; 3) initiates action potentials in inhibitory interneuron
s electrically coupled to the M-cell axon, and by their means inhibits a) inhibitory interneurons still at the same side of the body (to prevent them from interfering with the C-start), as well as b) motoneurons at the other side of the body. As a result of this pattern of activation the quick muscle
s at one side of the body contract simultaneously, while the muscles at the other side of the body relax.
s or electrical synaptic
coupling having low resistance gap junctions joining the cells. When the region of the PHP cell axon outside the axon cap depolarises, the influx of positive charge into the cell through voltage gated sodium channels is accompanied by a passive outflow of current from the PHP cell axon into the region bound by the axon cap. Due to the high resistance of the surrounding glial cells, the charge does not dissipate and the potential across the M-cell membrane is increased, hyperpolarising it.
and quasi-electrical (ephaptic
) synapses, the Mauthner cell has a strong field potential of a very characteristic shape. This field potential starts with a high-amplitude potential sink up to tens of mV
in amplitude that originates from the Mauthner cell discharge, and which is closely followed by a positive potential, called Extrinsic Hyperpolarizing Potential or EHP, which is associated with the activity of the recurrent feedback network.
Due to its high amplitude, in some animals the negative part of Mauthner cell field potential can be detected up to several hundred micrometres away from the cell itself. The positive components of the field potential are strongest in the axon cap, reaching amplitudes of 45 mV in adult goldfish. With a knowledge of these properties of the field potential, it is possible to use field potential monitoring as a way to find the Mauthner cell body in vivo
, or in vitro
in a whole brain preparation, moving the recording electrode in the hindbrain, while at the same time stimulating the spinal cord
, thus evoking antidromic
action potentials in the Mauthner cell axon.
was shown to increase inhibitory inputs to the M-cell, while application of dopamine
- to increase the amplitude of both chemical and electrical components of the VIIIth nerve responses via a G protein
-mediated activation of postsynaptic D2 receptor. An activity-dependent LTP
can be evoked in M-cells by a high-frequency stimulation of the VIIIth nerve. Surprisingly, this LTP is electrical synapse
-mediated, and is presumed to involve modification of the gap junction
channels. A possibility of LTP induction by sensory stimuli in vivo
, and the evidence for the LTP of inhibitory inputs to M-cells were also demonstrated.
Spontaneous preference in turn direction in young goldfish is correlated with one of the Mauthner cells being bigger than the other one. It is possible to change the preference of fish by raising them in conditions facilitating turns in a specific direction; this shift is accompanied by a correspondent change in M-cell sizes.
in the teleost fish for its associated neural circuit which mediates an escape response called the C-start or C-startle to direct the fish away from a predator.
The M-cell is a model system in the field of Neuroethology
. The M-cell system has served for detailed neurophysiological and histological investigations of synaptic transmission and synaptic plasticity
. Studies by Donald Faber and Henri Korn helped to establish the one vesicle
hypothesis of synaptic transmission in the CNS
. Other important research topics that have been investigated in the M-cell system include studies by Yoichi Oda and colleagues on inhibitory long-term potentiation
and auditory
conditioning
of the startle response, and studies by Alberto Pereda and colleagues on plasticity of electrical synapse
s. Other research topics investigated in the M-cell system include studies of spinal
neural networks and neural regeneration by Joe Fetcho and colleagues, as well as underwater sound localization
, and the biophysics of computation in single neurons.
Neuron
A neuron is an electrically excitable cell that processes and transmits information by electrical and chemical signaling. Chemical signaling occurs via synapses, specialized connections with other cells. Neurons connect to each other to form networks. Neurons are the core components of the nervous...
s (one for each half of the body) located in the rhombomere
Rhombomere
In the vertebrate embryo, a rhombomere is a transiently divided segment of the developing neural tube, within the hindbrain region in the area that will eventually become the rhombencephalon. The rhombomeres appear as a series of slightly constricted swellings in the neural tube, caudal to the...
4 of the hindbrain in fish and amphibian
Amphibian
Amphibians , are a class of vertebrate animals including animals such as toads, frogs, caecilians, and salamanders. They are characterized as non-amniote ectothermic tetrapods...
s that are responsible for a very fast escape reflex
Reflex
A reflex action, also known as a reflex, is an involuntary and nearly instantaneous movement in response to a stimulus. A true reflex is a behavior which is mediated via the reflex arc; this does not apply to casual uses of the term 'reflex'.-See also:...
(in the majority of animals - a so called C-start response). The cells are also notable for their unusual use of both chemical and electrical
Electrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
synapses.
Evolutionary history
Mauthner cells first appear in lampreys (being absent in hagfishHagfish
Hagfish, the clade Myxini , are eel-shaped slime-producing marine animals . They are the only living animals that have a skull but not a vertebral column. Along with lampreys, hagfish are jawless and are living fossils whose next nearest relatives include all vertebrates...
and lancelet
Lancelet
The lancelets , also known as amphioxus, are the modern representatives of the subphylum Cephalochordata, formerly thought to be the sister group of the craniates. They are usually found buried in sand in shallow parts of temperate or tropical seas. In Asia, they are harvested commercially as food...
s), and are present in virtually all teleost fish, as well as in amphibians (including postmetamorphic
Metamorphosis
Metamorphosis is a biological process by which an animal physically develops after birth or hatching, involving a conspicuous and relatively abrupt change in the animal's body structure through cell growth and differentiation...
anurans). Some fish, such as the lumpsuckers seem to have lost the Mauthner cells however.
The C-start
A C-start is a type of a very quick startle or escape reflexEscape reflex
Escape reflex, a kind of escape response, is a simple reflectory reaction in response to stimuli indicative of danger, that initiates an escape motion of an animal....
that is employed by fish and amphibian
Amphibian
Amphibians , are a class of vertebrate animals including animals such as toads, frogs, caecilians, and salamanders. They are characterized as non-amniote ectothermic tetrapods...
s (including larval
Larvae
In Roman mythology, lemures were shades or spirits of the restless or malignant dead, and are probably cognate with an extended sense of larvae as disturbing or frightening...
anurans). There are two sequential stages in the C-start: first, the head rotates about the center of mass
Center of mass
In physics, the center of mass or barycenter of a system is the average location of all of its mass. In the case of a rigid body, the position of the center of mass is fixed in relation to the body...
towards the direction of future escape, and the body of the animal exhibits a curvature that resembles a letter C; then, at the second stage, the animal is propelled forward. The duration of these stages varies from species to species from about 10 to 20 ms for the first stage, and from 20 to 30 ms for the second. In fish this forward propulsion does not require contraction of the antagonistic muscle
Muscle
Muscle is a contractile tissue of animals and is derived from the mesodermal layer of embryonic germ cells. Muscle cells contain contractile filaments that move past each other and change the size of the cell. They are classified as skeletal, cardiac, or smooth muscles. Their function is to...
, but results from the body stiffness and the hydrodynamic resistance of the tail
Tail
The tail is the section at the rear end of an animal's body; in general, the term refers to a distinct, flexible appendage to the torso. It is the part of the body that corresponds roughly to the sacrum and coccyx in mammals, reptiles, and birds...
. When an antagonistic muscular contraction does occur during stage 2, the fish rotates in the opposite direction, producing a counter-turn, and a directional change.
The role of the Mauthner cell in the C-start behavior
In cases when an abrupt acousticAcoustics
Acoustics is the interdisciplinary science that deals with the study of all mechanical waves in gases, liquids, and solids including vibration, sound, ultrasound and infrasound. A scientist who works in the field of acoustics is an acoustician while someone working in the field of acoustics...
, tactile or visual stimulus elicits a single action potential
Action potential
In physiology, an action potential is a short-lasting event in which the electrical membrane potential of a cell rapidly rises and falls, following a consistent trajectory. Action potentials occur in several types of animal cells, called excitable cells, which include neurons, muscle cells, and...
in one M-cell, it always correlates with a contralateral C-start escape. An extremely quick mutual feedback
Feedback
Feedback describes the situation when output from an event or phenomenon in the past will influence an occurrence or occurrences of the same Feedback describes the situation when output from (or information about the result of) an event or phenomenon in the past will influence an occurrence or...
inhibitory circuit then assures that 1) only one M-cell reaches spiking threshold, as the C-start has to be unilateral by definition, 2) that only one action potential is fired.
The Mauthner cell-mediated C-start reflex is very quick, with about 5-10 ms latency between the acoustic/tactile stimulus
Stimulus (physiology)
In physiology, a stimulus is a detectable change in the internal or external environment. The ability of an organism or organ to respond to external stimuli is called sensitivity....
and the Mauthner cell discharge, and only about 2 ms between the discharge and the unilateral muscle contraction. Mauthner cells is thus the quickest motor neuron to respond to the stimulus. It makes the C-start response behaviorally important as a way to initiate the escape reflex in an all or nothing fashion, while the direction and speed of the escape can be corrected later through the activity of smaller motor neurons.
In larval
Larvae
In Roman mythology, lemures were shades or spirits of the restless or malignant dead, and are probably cognate with an extended sense of larvae as disturbing or frightening...
zebrafish about ~60% of the total population of reticulospinal neurons are also activated by a stimulus that elicits the M-spike and C-start escape. A well-studied group of these reticulospinal neurons are the bilaterally paired M-cell homologues denoted MiD2cm and MiD3cm. These neurons exhibit morphological similarities to the M-cell including a lateral and ventral dendrite. They are located in rhombomere
Rhombomere
In the vertebrate embryo, a rhombomere is a transiently divided segment of the developing neural tube, within the hindbrain region in the area that will eventually become the rhombencephalon. The rhombomeres appear as a series of slightly constricted swellings in the neural tube, caudal to the...
s 5 and 6 of hindbrain respectively, and also receive auditory input in parallel with the M-cell from the pVIIIth nerve. In fish, water jet stimuli that activate these neurons elicit non-mauthner initiated C-starts of a longer latency, compared with M-cell associated ones.
Although the M-cell is often considered the prototype of a command neuron
Command neuron
A command neuron is a single neuron whose stimulation results in the evocation of an endogenous, specific, naturally occurring behavior pattern . Command neurons act as neural decision making cells; push buttons that can trigger a complete, coordinated behavioral act and are often the sole...
in vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
s, this designation may not be fully warranted. Although electrical stimulation of the M-cell is sufficient for eliciting a C-start, this C-start is normally weaker than the one evoked by a sensory stimulus. Moreover, the C-start can be evoked even with the M-cell ablated
Ablation
Ablation is removal of material from the surface of an object by vaporization, chipping, or other erosive processes. This occurs in spaceflight during ascent and atmospheric reentry, glaciology, medicine, and passive fire protection.-Spaceflight:...
, although in this case the latency of the response increases. The most widely accepted model of the M-cell system, or brainstem escape network, is that the M-cell initiates a fixed action pattern to the left or right by activating a spinal motor circuit initially described by J. Diamond and colleagues, but the precise trajectory of the escape is encoded by population activity in the other classes of reticulospinal neurons functioning in parallel to the M-cell. This notion is supported by studies using in vivo calcium imaging in larval zebrafish which show that MiD2cm and MiD3cm are activated along with the M-cell when an offending stimulus is directed towards the head but not the tail, and are correlated with C-starts of a larger initial turn angle.
Another component of the escape response is mediated by cranial relay neurons that are activated by the Mauthner cell spike. These neurons are electrically coupled with motoneurons which innervate extraocular, jaw and opercular muscles and mediate pectoral fin adduction in hatchetfish
Hatchetfish
The name hatchetfish may refer to two unrelated groups of fishes:*Marine hatchetfishes, small deep-sea bioluminescent fishes of the family Sternoptychidae, subfamily Sternoptychinae....
. This component of the neural circuit was first described by Michael V.L. Bennett and colleagues.
Mauthner cells in other types of behavior
Mauthner cells may be involved into behavioral patterns other than the C-start, if these types of behavior also require extremely quick bending movement of the body. Thus in goldfishGoldfish
The goldfish is a freshwater fish in the family Cyprinidae of order Cypriniformes. It was one of the earliest fish to be domesticated, and is one of the most commonly kept aquarium fish....
Mauthner cells are activated during prey capture near the surface of the water, as this type of hunting is dangerous for the fish, and it would benefit from leaving the surface as soon as possible after the prey is captured.
In adult postmetamorphic
Metamorphosis
Metamorphosis is a biological process by which an animal physically develops after birth or hatching, involving a conspicuous and relatively abrupt change in the animal's body structure through cell growth and differentiation...
anurans that do not have a tail, M-cells are nevertheless preserved and their discharges are associated with rapid movement of leg
Leg
Łęg may refer to the following places in Poland:*A former name for the town of Ełk *Part of the Czyżyny district of Kraków*Łęg, Pleszew County in Greater Poland Voivodeship...
s during an escape.
Inputs to the M-cell: excitation and feed forward inhibition
The M-cell has two primary aspiny dendriteDendrite
Dendrites are the branched projections of a neuron that act to conduct the electrochemical stimulation received from other neural cells to the cell body, or soma, of the neuron from which the dendrites project...
s which receive segregated inputs from various parts of the neural system. One dendrite projects laterally and the other projects either in the ventral or medial direction, depending on the species.
The ventral dendrite receives information from the optic tectum and spinal cord
Spinal cord
The spinal cord is a long, thin, tubular bundle of nervous tissue and support cells that extends from the brain . The brain and spinal cord together make up the central nervous system...
while the lateral dendrite receives inputs from the octovolateralis systems (the lateral line
Lateral line
The lateral line is a sense organ in aquatic organisms , used to detect movement and vibration in the surrounding water. Lateral lines are usually visible as faint lines running lengthwise down each side, from the vicinity of the gill covers to the base of the tail...
, accoustic inputs from the inner ear
Inner ear
The inner ear is the innermost part of the vertebrate ear. In mammals, it consists of the bony labyrinth, a hollow cavity in the temporal bone of the skull with a system of passages comprising two main functional parts:...
, and inertial information from the statoliths brought by the cranial nerve VIII).
The fibers from the ipsilateral cranial nerve VIII terminate in excitatory mixed electrical
Electrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
and glutamatergic synapses on the M-cell. They also electrically activate glycine
Glycine
Glycine is an organic compound with the formula NH2CH2COOH. Having a hydrogen substituent as its 'side chain', glycine is the smallest of the 20 amino acids commonly found in proteins. Its codons are GGU, GGC, GGA, GGG cf. the genetic code.Glycine is a colourless, sweet-tasting crystalline solid...
rgic inhibitory interneurons that terminate on the M-cells. Despite the inhibitory input having one more synapse in its pathway, there is no delay between the excitation and inhibition because the intervening synapse is electrical. It was shown that for weak stimuli the inhibition wins over the excitation, preventing the M-cell from a discharge, while for stronger stimuli excitation becomes dominant. The Inner ear
Inner ear
The inner ear is the innermost part of the vertebrate ear. In mammals, it consists of the bony labyrinth, a hollow cavity in the temporal bone of the skull with a system of passages comprising two main functional parts:...
afferents also terminate with electrical synapses on a population PHP inhibitory interneurons (see below) to provide an additional level of feed forward inhibition. The Mauthner cell also has GABA
Gabâ
Gabâ or gabaa, for the people in many parts of the Philippines), is the concept of a non-human and non-divine, imminent retribution. A sort of negative karma, it is generally seen as an evil effect on a person because of their wrongdoings or transgressions...
-, dopamine
Dopamine
Dopamine is a catecholamine neurotransmitter present in a wide variety of animals, including both vertebrates and invertebrates. In the brain, this substituted phenethylamine functions as a neurotransmitter, activating the five known types of dopamine receptors—D1, D2, D3, D4, and D5—and their...
-, serotonin
Serotonin
Serotonin or 5-hydroxytryptamine is a monoamine neurotransmitter. Biochemically derived from tryptophan, serotonin is primarily found in the gastrointestinal tract, platelets, and in the central nervous system of animals including humans...
- and somatostatin
Somatostatin
Somatostatin is a peptide hormone that regulates the endocrine system and affects neurotransmission and cell proliferation via interaction with G-protein-coupled somatostatin receptors and inhibition of the release of numerous secondary hormones.Somatostatin...
ergic inputs, each restricted to certain dendritic region.
Inputs from the optic tectum and the lateral line help control which way the C-startle bends by biasing the mauthner cells when there are obstacles in the vicinity. In cases where movement away from the stimulus is blocked, the fish way bend towards the disturbance.
Axon cap
The Mauthner cell axon hillockAxon hillock
The axon hillock is a specialized part of the cell body of a neuron that connects to the axon. As a result, the axon hillock is the last site in the soma where membrane potentials propagated from synaptic inputs are summated before being transmitted to the axon. For many years it was believed...
is surrounded by a dense formation of neuropil, called the Axon cap. The high resistance of this axon cap contributes to the typical shape of the Mauthner cell field potential (see below). It its most advanced form the axon cap consists of a core, immediately adjacent to the Mauthner cell axon, and containing a network of very thin unmyelinated
Myelin
Myelin is a dielectric material that forms a layer, the myelin sheath, usually around only the axon of a neuron. It is essential for the proper functioning of the nervous system. Myelin is an outgrowth of a type of glial cell. The production of the myelin sheath is called myelination...
fibers, and a peripheral part. This peripheral part contains the large unmyelinated fibers of the PHP neurons (see below) that mediate the inhibitory feedback to the Mauthner cell; the Mauthner cell itself also sends small dendrites from its axon hill to the peripheral part of the axon cap. Finally, the surface of the axon cap is covered with a cap wall composed of several layers of astrocyte
Astrocyte
Astrocytes , also known collectively as astroglia, are characteristic star-shaped glial cells in the brain and spinal cord...
-like glial cells. Both glial cells and the unmyelinated fibers are coupled with each other by means of gap junction
Gap junction
A gap junction or nexus is a specialized intercellular connection between a multitude of animal cell-types. It directly connects the cytoplasm of two cells, which allows various molecules and ions to pass freely between cells....
s.
Evolutionary the axon cap is a more recent development than the Mauthner cell itself, so some animals, such as lamprey
Lamprey
Lampreys are a family of jawless fish, whose adults are characterized by a toothed, funnel-like sucking mouth. Translated from an admixture of Latin and Greek, lamprey means stone lickers...
s and eel
Eel
Eels are an order of fish, which consists of four suborders, 20 families, 111 genera and approximately 800 species. Most eels are predators...
s, while having functional Mauthner cells, don't have axon cap at all, while some other animals, such as amphibia and lungfish
Lungfish
Lungfish are freshwater fish belonging to the Subclass Dipnoi. Lungfish are best known for retaining characteristics primitive within the Osteichthyes, including the ability to breathe air, and structures primitive within Sarcopterygii, including the presence of lobed fins with a well-developed...
, do have a very simplified version of it.
Feedback network
The main part of the Mauthner cell-associated network is the negative feedbackFeedback
Feedback describes the situation when output from an event or phenomenon in the past will influence an occurrence or occurrences of the same Feedback describes the situation when output from (or information about the result of) an event or phenomenon in the past will influence an occurrence or...
network, which assures that a) only one of the two Mauthner cells fires in response to the stimulus; b) the Mauthner cell that fires, does it only once. Both these requirements are quite natural considering that the consequences of a single Mauthner cell discharge are so strong; a failure to comply with these two rules would not only prevent the animal from escaping, but could even physically damage it. The fastest part of this negative feedback network, which is also the one closest to the Mauthner cell, is that of the so called passive hyperpolarizing field potential or PHP neurons. The fibers of these neurons are located in the axon cap, and they receive inputs from both ipsilateral and contralateral Mauthner cells. The field potentials of PHP neurons are strongly positive, and form a part of the 'Signature field potential' of the Mauthner cell (see below), with the early (ipsilaterally initiated) component being called the Extracellular Hyperpolarizing Potential (EHP), and the later (contralaterally initiated) component being sometimes addressed in the literature as the Late Collateral Inhibition (LCI). The action of PHP neurons onto the Mauthner cells is mediated by electrical, and not chemical effects: the outward currents generated by the action potential
Action potential
In physiology, an action potential is a short-lasting event in which the electrical membrane potential of a cell rapidly rises and falls, following a consistent trajectory. Action potentials occur in several types of animal cells, called excitable cells, which include neurons, muscle cells, and...
s in axon cap fibers flow inward across the Mauthner cell axon hillock
Axon hillock
The axon hillock is a specialized part of the cell body of a neuron that connects to the axon. As a result, the axon hillock is the last site in the soma where membrane potentials propagated from synaptic inputs are summated before being transmitted to the axon. For many years it was believed...
and hyperpolarize it.
Outputs
The only axonAxon
An axon is a long, slender projection of a nerve cell, or neuron, that conducts electrical impulses away from the neuron's cell body or soma....
of the Mauthner cell reaches from the cell to the midline of the hindbrain, promptly crosses it to the contralateral side, and then descends caudally along the spinal cord
Spinal cord
The spinal cord is a long, thin, tubular bundle of nervous tissue and support cells that extends from the brain . The brain and spinal cord together make up the central nervous system...
. A single discharge of the M-cell achieves a whole set of parallel effects onto the spinal motor networks: 1) it monosynaptically excites large primary motoneurons at one side of the body; 2) disinaptically excites smaller motoneurons at the same side of the body; 3) initiates action potentials in inhibitory interneuron
Interneuron
An interneuron is a multipolar neuron which connects afferent neurons and efferent neurons in neural pathways...
s electrically coupled to the M-cell axon, and by their means inhibits a) inhibitory interneurons still at the same side of the body (to prevent them from interfering with the C-start), as well as b) motoneurons at the other side of the body. As a result of this pattern of activation the quick muscle
Muscle
Muscle is a contractile tissue of animals and is derived from the mesodermal layer of embryonic germ cells. Muscle cells contain contractile filaments that move past each other and change the size of the cell. They are classified as skeletal, cardiac, or smooth muscles. Their function is to...
s at one side of the body contract simultaneously, while the muscles at the other side of the body relax.
Ephaptic properties
The inhibition of the M-cell by the PHP cells occurs by ephaptic interactions. The inhibition is brought about without a chemical synapseChemical synapse
Chemical synapses are specialized junctions through which neurons signal to each other and to non-neuronal cells such as those in muscles or glands. Chemical synapses allow neurons to form circuits within the central nervous system. They are crucial to the biological computations that underlie...
s or electrical synaptic
Electrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
coupling having low resistance gap junctions joining the cells. When the region of the PHP cell axon outside the axon cap depolarises, the influx of positive charge into the cell through voltage gated sodium channels is accompanied by a passive outflow of current from the PHP cell axon into the region bound by the axon cap. Due to the high resistance of the surrounding glial cells, the charge does not dissipate and the potential across the M-cell membrane is increased, hyperpolarising it.
Signature field potential
Because of its size, presence of a quick feedback network, and abundance of electricalElectrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
and quasi-electrical (ephaptic
Ephaptic coupling
Ephaptic coupling is indirect communication within the nervous system through extracellular electric fields, as opposed to direct communication via electrical synapses or chemical synapses. Ephaptic communication has been observed in myelinated nerve fibers....
) synapses, the Mauthner cell has a strong field potential of a very characteristic shape. This field potential starts with a high-amplitude potential sink up to tens of mV
MV
-Science and technology:* Maedi-visna virus or visna virus, a virus causing encephalitis and pneumonitis in sheep and goats* Materialized view, a concept in database management systems...
in amplitude that originates from the Mauthner cell discharge, and which is closely followed by a positive potential, called Extrinsic Hyperpolarizing Potential or EHP, which is associated with the activity of the recurrent feedback network.
Due to its high amplitude, in some animals the negative part of Mauthner cell field potential can be detected up to several hundred micrometres away from the cell itself. The positive components of the field potential are strongest in the axon cap, reaching amplitudes of 45 mV in adult goldfish. With a knowledge of these properties of the field potential, it is possible to use field potential monitoring as a way to find the Mauthner cell body in vivo
In vivo
In vivo is experimentation using a whole, living organism as opposed to a partial or dead organism, or an in vitro controlled environment. Animal testing and clinical trials are two forms of in vivo research...
, or in vitro
In vitro
In vitro refers to studies in experimental biology that are conducted using components of an organism that have been isolated from their usual biological context in order to permit a more detailed or more convenient analysis than can be done with whole organisms. Colloquially, these experiments...
in a whole brain preparation, moving the recording electrode in the hindbrain, while at the same time stimulating the spinal cord
Spinal cord
The spinal cord is a long, thin, tubular bundle of nervous tissue and support cells that extends from the brain . The brain and spinal cord together make up the central nervous system...
, thus evoking antidromic
Antidromic
An antidromic impulse in an axon refers to conduction opposite of the normal direction. That is, it refers to conduction along the axon away from the axon terminal and towards the soma...
action potentials in the Mauthner cell axon.
Plasticity
Application of serotoninSerotonin
Serotonin or 5-hydroxytryptamine is a monoamine neurotransmitter. Biochemically derived from tryptophan, serotonin is primarily found in the gastrointestinal tract, platelets, and in the central nervous system of animals including humans...
was shown to increase inhibitory inputs to the M-cell, while application of dopamine
Dopamine
Dopamine is a catecholamine neurotransmitter present in a wide variety of animals, including both vertebrates and invertebrates. In the brain, this substituted phenethylamine functions as a neurotransmitter, activating the five known types of dopamine receptors—D1, D2, D3, D4, and D5—and their...
- to increase the amplitude of both chemical and electrical components of the VIIIth nerve responses via a G protein
G protein
G proteins are a family of proteins involved in transmitting chemical signals outside the cell, and causing changes inside the cell. They communicate signals from many hormones, neurotransmitters, and other signaling factors. G protein-coupled receptors are transmembrane receptors...
-mediated activation of postsynaptic D2 receptor. An activity-dependent LTP
Long-term potentiation
In neuroscience, long-term potentiation is a long-lasting enhancement in signal transmission between two neurons that results from stimulating them synchronously. It is one of several phenomena underlying synaptic plasticity, the ability of chemical synapses to change their strength...
can be evoked in M-cells by a high-frequency stimulation of the VIIIth nerve. Surprisingly, this LTP is electrical synapse
Electrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
-mediated, and is presumed to involve modification of the gap junction
Gap junction
A gap junction or nexus is a specialized intercellular connection between a multitude of animal cell-types. It directly connects the cytoplasm of two cells, which allows various molecules and ions to pass freely between cells....
channels. A possibility of LTP induction by sensory stimuli in vivo
In vivo
In vivo is experimentation using a whole, living organism as opposed to a partial or dead organism, or an in vitro controlled environment. Animal testing and clinical trials are two forms of in vivo research...
, and the evidence for the LTP of inhibitory inputs to M-cells were also demonstrated.
Spontaneous preference in turn direction in young goldfish is correlated with one of the Mauthner cells being bigger than the other one. It is possible to change the preference of fish by raising them in conditions facilitating turns in a specific direction; this shift is accompanied by a correspondent change in M-cell sizes.
History of research
The Mauthner cell was first identified by the Viennese ophthalmologist Ludwig MauthnerLudwig Mauthner
Ludwig Mauthner was an Austrian neuroanatomist and ophthalmologist who was a native of Prague.He studied medicine at the University of Vienna, where he received his doctorate in 1861. In 1864 he was a privatdozent of ophthalmology, and in 1869 became a professor at the University of Innsbruck...
in the teleost fish for its associated neural circuit which mediates an escape response called the C-start or C-startle to direct the fish away from a predator.
The M-cell is a model system in the field of Neuroethology
Neuroethology
Neuroethology is the evolutionary and comparative approach to the study of animal behavior and its underlying mechanistic control by the nervous system...
. The M-cell system has served for detailed neurophysiological and histological investigations of synaptic transmission and synaptic plasticity
Synaptic plasticity
In neuroscience, synaptic plasticity is the ability of the connection, or synapse, between two neurons to change in strength in response to either use or disuse of transmission over synaptic pathways. Plastic change also results from the alteration of the number of receptors located on a synapse...
. Studies by Donald Faber and Henri Korn helped to establish the one vesicle
Synaptic vesicle
In a neuron, synaptic vesicles store various neurotransmitters that are released at the synapse. The release is regulated by a voltage-dependent calcium channel. Vesicles are essential for propagating nerve impulses between neurons and are constantly recreated by the cell...
hypothesis of synaptic transmission in the CNS
Central nervous system
The central nervous system is the part of the nervous system that integrates the information that it receives from, and coordinates the activity of, all parts of the bodies of bilaterian animals—that is, all multicellular animals except sponges and radially symmetric animals such as jellyfish...
. Other important research topics that have been investigated in the M-cell system include studies by Yoichi Oda and colleagues on inhibitory long-term potentiation
Long-term potentiation
In neuroscience, long-term potentiation is a long-lasting enhancement in signal transmission between two neurons that results from stimulating them synchronously. It is one of several phenomena underlying synaptic plasticity, the ability of chemical synapses to change their strength...
and auditory
Audition
An audition is a sample performance by an actor, singer, musician, dancer or other performing artist.Audition may also refer to:* The sense of hearing* Adobe Audition, audio editing software...
conditioning
Conditioning
Conditioning may refer to:* In psychology, the process of performing some particular action to directly influence an individual's learning; see education...
of the startle response, and studies by Alberto Pereda and colleagues on plasticity of electrical synapse
Electrical synapse
An electrical synapse is a mechanical and electrically conductive link between two abutting neurons that is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.5 nm of each other, a much shorter...
s. Other research topics investigated in the M-cell system include studies of spinal
Vertebral column
In human anatomy, the vertebral column is a column usually consisting of 24 articulating vertebrae, and 9 fused vertebrae in the sacrum and the coccyx. It is situated in the dorsal aspect of the torso, separated by intervertebral discs...
neural networks and neural regeneration by Joe Fetcho and colleagues, as well as underwater sound localization
Sound localization
Sound localization refers to a listener's ability to identify the location or origin of a detected sound in direction and distance. It may also refer to the methods in acoustical engineering to simulate the placement of an auditory cue in a virtual 3D space .The sound localization mechanisms of the...
, and the biophysics of computation in single neurons.