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TheMauthner cellsare a pair of big and easily identifiableneurons(one for each half of the body) located in therhombomere4 of thehindbrainin fish andamphibiansthat are responsible for a very fast escapereflex(in the majority of animals – a so-called C-start response). The cells are also notable for their unusual use of both chemical andelectricalsynapses.[1]

Evolutionary history[edit]

Mauthner cells first appear inlampreys(being absent inhagfishandlancelets),[2]and are present in virtually allteleostfish, as well as inamphibians(includingpostmetamorphicfrogsandtoads[3]). Some fish, such aslumpsuckers,seem to have lost the Mauthner cells however.[4]

Role in behavior[edit]

The C-start[edit]

A C-start is a type of a very quick startle orescape reflexthat is employed byfishandamphibians(includinglarvalfrogsand toads). There are two sequential stages in the C-start: first, the head rotates about thecenter of masstowards 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.[5]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.[1][4]In fish this forward propulsion does not require contraction of the antagonisticmuscle,but results from the body stiffness and thehydrodynamicresistance of thetail.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[edit]

In cases when an abruptacoustic,tactileorvisualstimulus elicits a singleaction potentialin one M-cell, it always correlates with acontralateralC-start escape.[6]An extremely quick mutualfeedbackinhibitorycircuit then assures that only one M-cell reaches spiking threshold—as the C-start has to beunilateralby definition—and that only one action potential is fired.[1]

The Mauthner cell-mediated C-start reflex is very quick, with about 5-10 ms latency between the acoustic/tactilestimulusand the Mauthner cell discharge, and only about 2 ms between the discharge and the unilateral muscle contraction.[1][6]Mauthner cells are 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 anall or nothingfashion, while the direction and speed of the escape can be corrected later through the activity of smaller motor neurons.

Inlarvalzebrafishabout ~60% of the total population ofreticulospinalneurons 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-cellhomologuesdenotedMiD2cmandMiD3cm.These neurons exhibit morphological similarities to the M-cell including a lateral and ventral dendrite. They are located inrhombomeres5 and 6 ofhindbrainrespectively, and also receive auditory input in parallel with the M-cell from thepVIIIth 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 acommand neuroninvertebrates,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.[7]Moreover, the C-start can be evoked even with the M-cellablated,although in this case the latency of the response increases.[8]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 usingin vivocalcium imaging in larval zebrafish which show thatMiD2cmandMiD3cmare 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 bycranial relay neuronsthat 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 inhatchetfish.[9][10]This component of the neural circuit was first described by Michael V.L. Bennett and colleagues.

Mauthner cells in other types of behavior[edit]

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 ingoldfishMauthner 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.[11]

In adultpostmetamorphicanurans(frogs and toads) that do not have a tail, M-cells are nevertheless preserved[3]and their discharges are associated with rapid movement oflegsduring an escape.[12]In addition, larvallampreys(eel-like jawless fish of superclass Cyclostomata) exhibit rapid withdrawal behavior that is correlated with Mauthner cell activity and involves bilateral, posture-dependent muscular contractions along the length of the body.[13]Larval lampreys (ammocoetes) are filter feeders that occupy crescent-shaped burrows in the silt or mud bottoms of freshwater stream beds, with their mouths positioned at, or just above the surface of the mud. Sudden vibration activates both Mauthner neurons in the lamprey brainstem, which causes an accordion-like muscular contraction in the trunk and tail and pulls the head down into the burrow.

Morphology and connections[edit]

Inputs to the M-cell: excitation and feed forward inhibition[edit]

The M-cell has two primary aspiny (lackingdendritic spines)dendriteswhich receive segregated inputs from various parts of the neural system.[1]One dendrite projects laterally and the other projects either in the ventral or medial direction, depending on the species.[14]

The ventral dendrite receives information from theoptic tectum[15]andspinal cord[16]while the lateral dendrite receives inputs from the octovolateralis systems (thelateral line,acoustic inputs from theinner ear,and inertial information from the statoliths brought by thecranial nerve VIII).[1]

The fibers from theipsilateralcranial nerve VIII terminate in excitatory mixedelectricalandglutamatergicsynapseson the M-cell. They also electrically activateglycinergicinhibitory 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.[17]TheInner earafferents 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 hasGABA-,dopamine-,serotonin- andsomatostatinergicinputs, each restricted to certain dendritic region.[1]

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 may bend towards the disturbance.[1][18]

Axon cap[edit]

The Mauthner cellaxon hillockis surrounded by a dense formation of neuropil, called theaxon cap.[2]The high resistance of this axon cap contributes to the typical shape of the Mauthner cell field potential (see below). In its most advanced form the axon cap consists of a core, immediately adjacent to the Mauthner cell axon, and containing a network of very thinunmyelinatedfibers, 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 acap wallcomposed of several layers ofastrocyte-likeglialcells. Both glial cells and the unmyelinated fibers are coupled with each other by means ofgap junctions.[19]

Evolutionarily, the axon cap is a more recent development than the Mauthner cell itself, so some animals, such aslampreysandeels,while having functional Mauthner cells, don't have axon cap at all, while some other animals, such asamphibiaandlungfish,do have a very simplified version of it.[2]

Feedback network[edit]

The main part of the Mauthner cell-associated network is the negativefeedbacknetwork, which assures that only one of the two Mauthner cells fires in response to the stimulus and that, whichever Mauthner cell fires, it does so 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-calledpassive hyperpolarizing field potentialorPHP neurons.[1]The fibers of these neurons are located in the axon cap, and they receive inputs from bothipsilateralandcontralateralMauthner cells. Thefield potentialsof 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).[19]The action of PHP neurons onto the Mauthner cells is mediated by electrical, and not chemical effects: the outward currents generated by theaction potentialsin axon cap fibers flow inward across the Mauthner cellaxon hillockand hyperpolarize it.[1]

Outputs[edit]

The onlyaxonof the Mauthner cell reaches from the cell to the midline of thehindbrain,promptly crosses it to the contralateral side, and then descends caudally along thespinal cord.[19]A single discharge of the M-cell achieves a whole set of parallel effects onto the spinal motor networks: 1) it monosynaptically excites large primarymotoneuronsat one side of the body; 2) disynaptically excites smaller motoneurons at the same side of the body; 3) initiates action potentials in inhibitoryinterneuronselectrically 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 quickmusclesat one side of the body contract simultaneously, while the muscles at the other side of the body relax.[20]

Electrophysiology[edit]

Ephaptic properties[edit]

Ephaptic inhibition at the mauthner axon cap by PHP cells

The inhibition of the M-cell by the PHP cells occurs byephaptic interactions.The inhibition is brought about without achemical synapsesorelectrical synapticcoupling having low resistancegap junctionsjoining the cells. When the region of the PHP cell axon outside the axon cap depolarizes, the influx of positive charge into the cell throughvoltage gated sodium channelsis 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, hyperpolarizing it.

Signature field potential[edit]

Because of its size, presence of a quick feedback network, and abundance ofelectricaland quasi-electrical (ephaptic) synapses, the Mauthner cell has a strongfield potentialof a very characteristic shape.[6][19]This field potential starts with a high-amplitude potential sink up to tens ofmillivoltsin 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.[1]

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.[6]The positive components of the field potential are strongest in the axon cap, reaching amplitudes of 45 mV in adult goldfish.[19]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 bodyin vivo,orin vitroin a whole brain preparation, moving the recording electrode in thehindbrain,while at the same time stimulating thespinal cord,thus evokingantidromicaction potentials in the Mauthner cell axon.[19]

Plasticity[edit]

Application ofserotoninwas shown to increase inhibitory inputs to the M-cell, while application ofdopamine– to increase the amplitude of both chemical and electrical components of the VIIIth nerve responses via aG protein-mediated activation of postsynapticD2 receptor.[1]An activity-dependentLTPcan be evoked in M-cells by a high-frequency stimulation of the VIIIth nerve. Surprisingly, this LTP iselectrical synapse-mediated, and is presumed to involve modification of thegap junctionchannels.[1]A possibility ofLTP inductionby sensory stimuliin vivo,[1]and the evidence for the LTP of inhibitory inputs to M-cells[17]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.[21]

History of research[edit]

The Mauthner cell was first identified by the Viennese ophthalmologistLudwig Mauthnerin theteleostfish for its associated neural circuit which mediates an escape response called the C-start or C-startleto direct the fish away from a predator.

The M-cell is a model system in the field ofNeuroethology.The M-cell system has served for detailedneurophysiologicalandhistologicalinvestigations ofsynaptic transmissionandsynaptic plasticity.[1]Studies byDonald FaberandHenri Kornhelped to establish the onevesiclehypothesis ofsynaptic transmissionin theCNS.Other important research topics that have been investigated in the M-cell system include studies byYoichi Odaand colleagues on inhibitorylong-term potentiationandauditoryconditioningof the startle response, and studies byAlberto Peredaand colleagues on plasticity ofelectrical synapses.Other research topics investigated in the M-cell system include studies ofspinalneural networks and neural regeneration byJoe Fetchoand colleagues, as well as underwatersound localization,and the biophysics of computation in single neurons.

References[edit]

  1. ^abcdefghijklmnoKorn H, Faber DS (July 2005)."The Mauthner cell half a century later: a neurobiological model for decision-making?".Neuron.47(1): 13–28.doi:10.1016/j.neuron.2005.05.019.PMID15996545.
  2. ^abcBierman HS, Zottoli SJ, Hale ME (2009). "Evolution of the Mauthner axon cap".Brain Behav. Evol.73(3): 174–87.doi:10.1159/000222562.PMID19494486.S2CID25637965.
  3. ^abWill U (February 1986). "Mauthner neurons survive metamorphosis in anurans: a comparative HRP study on the cytoarchitecture of Mauthner neurons in amphibians".J. Comp. Neurol.244(1): 111–20.doi:10.1002/cne.902440109.PMID3081602.S2CID40706257.
  4. ^abHale ME (October 2000). "Startle responses of fish without Mauthner neurons: escape behavior of the lumpfish (Cyclopterus lumpus)".Biol. Bull.199(2): 180–2.doi:10.2307/1542886.JSTOR1542886.PMID11081724.
  5. ^Eaton RC, DiDomenico R, Nissanov J (August 1988)."Flexible body dynamics of the goldfish C-start: implications for reticulospinal command mechanisms".J. Neurosci.8(8): 2758–68.doi:10.1523/JNEUROSCI.08-08-02758.1988.PMC6569417.PMID3411353.
  6. ^abcdZottoli SJ (February 1977)."Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish".J. Exp. Biol.66(1): 243–54.doi:10.1242/jeb.66.1.243.PMID858992.
  7. ^Nissanov J, Eaton RC, DiDomenico R (May 1990). "The motor output of the Mauthner cell, a reticulospinal command neuron".Brain Res.517(1–2): 88–98.doi:10.1016/0006-8993(90)91012-6.PMID2376010.S2CID28611729.
  8. ^Eaton RC, Lavender WA, Wieland CM (1982). "Alternative neural pathways initiate fast-start responses following lesions of the mauthner neuron in goldfish".J. Comp. Physiol.145(4): 485–496.doi:10.1007/BF00612814.S2CID8529312.
  9. ^Auerbach AA, Bennett MV (February 1969)."Chemically mediated transmission at a giant fiber synapse in the central nervous system of a vertebrate".The Journal of General Physiology.53(2): 183–210.doi:10.1085/jgp.53.2.183.PMC2202901.PMID4303656.
  10. ^Eaton RC, Bombardieri RA, Meyer DL (February 1977)."The Mauthner-initiated startle response in teleost fish".The Journal of Experimental Biology.66(1): 65–81.doi:10.1242/jeb.66.1.65.PMID870603.
  11. ^Canfield JG, Rose GJ (1993). "Activation of Mauthner neurons during prey capture".Journal of Comparative Physiology A.172(5): 611–618.doi:10.1007/BF00213683.S2CID20259458.
  12. ^Will U (1991). "Amphibian Mauthner cells".Brain Behav. Evol.37(5): 317–32.doi:10.1159/000114368.PMID1657273.
  13. ^Currie, SN (1991)."Vibration-evoked startle behavior in larval lampreys".Brain Behav Evol.37(5): 260–271.doi:10.1159/000114364.PMID1933250.
  14. ^Zottoli SJ, Faber DS (1 November 2000). "The Mauthner Cell: What Has It Taught Us?".Neuroscientist.6:26–38.CiteSeerX10.1.1.116.1442.doi:10.1177/107385840000600111.S2CID14633326.
  15. ^Zottoli SJ, Hordes AR, Faber DS (January 1987). "Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell".Brain Res.401(1): 113–21.doi:10.1016/0006-8993(87)91170-X.PMID3815088.S2CID33442056.
  16. ^Chang YT, Lin JW, Faber DS (August 1987). "Spinal inputs to the ventral dendrite of the teleost Mauthner cell".Brain Res.417(2): 205–13.doi:10.1016/0006-8993(87)90444-6.PMID3651811.S2CID23825121.
  17. ^abOda Y, Charpier S, Murayama Y, Suma C, Korn H (September 1995). "Long-term potentiation of glycinergic inhibitory synaptic transmission".J. Neurophysiol.74(3): 1056–74.doi:10.1152/jn.1995.74.3.1056.PMID7500132.
  18. ^Eaton RC, Emberley DS (November 1991)."How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish".The Journal of Experimental Biology.161(1): 469–87.doi:10.1242/jeb.161.1.469.PMID1757775.
  19. ^abcdefZottoli SJ, Wong TW, Agostini MA, Meyers JR (July 2011). "Axon cap morphology of the sea robin (Prionotus carolinus): mauthner cell is correlated with the presence of" signature "field potentials and a C-Type startle response".J. Comp. Neurol.519(10): 1979–98.doi:10.1002/cne.22617.PMID21452211.S2CID27602754.
  20. ^Fetcho JR (1991). "Spinal network of the Mauthner cell".Brain Behav. Evol.37(5): 298–316.doi:10.1159/000114367.PMID1933252.
  21. ^Shtanchaev RS, Mikhailova GZ, Dektyareva NY, Kokanova NA, Moshkov DA (November 2008). "Changes in the ventral dendrite of Mauthner neurons in goldfish after optokinetic stimulation".Neurosci. Behav. Physiol.38(9): 917–21.doi:10.1007/s11055-008-9071-9.PMID18975109.S2CID31352657.

Further reading[edit]

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