Initiation of Mauthner- or Non-Mauthner-Mediated Fast Escape Evoked by Different Modes of Sensory Input

Brainstem reticulospinal neurons (RSNs) serve as the major descending system in vertebrate sensorimotor integration. One of the paired RSNs in zebrafish, the Mauthner (M) cell, is thought to initiate fast escape from sudden noxious stimuli. Two other paired RSNs, morphologically homologous to the M-cell, are also suggested to play key roles in controlling fast escape. However, the relationship among activities of the M-cell and its homologs during fast escape and the sensory inputs that elicit escape via their activation are unclear. We have monitored hindbrain RSN activity simultaneously with tail flip movement during fast escape in zebrafish. Confocal calcium imaging of RSNs was performed on larvae rostrally embedded in agar but with their tails allowed to move freely. Application of a pulsed waterjet to the otic vesicle (OV) to activate acousticovestibular input elicited contralateral fast tail flips with short latency and an apparent Ca2+ increase, reflecting a single action potential, in the ipsilateral M-cell (M-escape). Application of waterjet to head skin for tactile stimulation elicited fast escapes, but onset was delayed and the M-cell did not fire (non-M-escape). After eliminating either the M-cell or OV, only non-M-escape was initiated. Simultaneous high-speed confocal imaging of the M-cell and one of its homologs, MiD3cm, revealed complementary activation during fast escape: MiD3cm activity was low during M-escape but high during non-M-escape. These results suggest that M-cell firing is necessary for fast escape with short latency elicited by acousticovestibular input and that MiD3cm is more involved in non-M-escape driven by head-tactile input.

[1]  Robert C. Eaton,et al.  Lateralization and adaptation of a continuously variable behavior following lesions of a reticulospinal command neuron , 1988, Brain Research.

[2]  J T Corwin,et al.  Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Sten Grillner,et al.  Initiation of locomotion , 1999 .

[4]  G. Viana di Prisco,et al.  Quantitative investigation of calcium signals for locomotor pattern generation in the lamprey spinal cord. , 2004, Journal of neurophysiology.

[5]  J. Fetcho Spinal Network of the Mauthner Cell (Part 1 of 2) , 1991 .

[6]  E. Furshpan,et al.  Two inhibitory mechanisms in the Mauthner neurons of goldfish. , 1963, Journal of neurophysiology.

[7]  J. Webb,et al.  Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[8]  P. Drapeau,et al.  Time course of the development of motor behaviors in the zebrafish embryo. , 1998, Journal of neurobiology.

[9]  J. T. Hackett,et al.  Mauthner axon networks mediating supraspinal components of the startle response in the goldfish , 1983, Neuroscience.

[10]  Herwig Baier,et al.  Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum , 2005, The Journal of Neuroscience.

[11]  Kristen E. Severi,et al.  Control of visually guided behavior by distinct populations of spinal projection neurons , 2008, Nature Neuroscience.

[12]  Robert C. Eaton,et al.  Identification of Mauthner-initiated response patterns in goldfish: Evidence from simultaneous cinematography and electrophysiology , 1981, Journal of comparative physiology.

[13]  J Nissanov,et al.  Flexible body dynamics of the goldfish C-start: implications for reticulospinal command mechanisms , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  J. T. Corwin,et al.  Lighting up the Senses: FM1-43 Loading of Sensory Cells through Nonselective Ion Channels , 2003, The Journal of Neuroscience.

[15]  Y. Oda,et al.  In Vivo Imaging of Functional Inhibitory Networks on the Mauthner Cell of Larval Zebrafish , 2002, The Journal of Neuroscience.

[16]  S. Grillner,et al.  Neural bases of goal-directed locomotion in vertebrates—An overview , 2008, Brain Research Reviews.

[17]  E. Furshpan,et al.  Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. , 1962, Journal of neurophysiology.

[18]  R. Yuste,et al.  Detecting action potentials in neuronal populations with calcium imaging. , 1999, Methods.

[19]  W. K. Metcalfe,et al.  T reticular interneurons: A class of serially repeating cells in the zebrafish hindbrain , 1985, The Journal of comparative neurology.

[20]  C. Kimmel,et al.  Functional development in the Mauthner cell system of embryos and larvae of the zebra fish. , 1977, Journal of neurobiology.

[21]  H. Kennedy,et al.  FM1-43 Dye Behaves as a Permeant Blocker of the Hair-Cell Mechanotransducer Channel , 2001, The Journal of Neuroscience.

[22]  S. Rossignol,et al.  Dynamic sensorimotor interactions in locomotion. , 2006, Physiological reviews.

[23]  R. C. Eaton,et al.  Identifiable reticulospinal neurons of the adult zebrafish, Brachydanio rerio , 1991, The Journal of comparative neurology.

[24]  R. Dampney,et al.  Functional organization of central pathways regulating the cardiovascular system. , 1994, Physiological reviews.

[25]  C. Kimmel,et al.  Decreased fast-start performance of zebrafish larvae lacking mauthner neurons , 1980, Journal of comparative physiology.

[26]  S. Grillner,et al.  Lateral turns in the Lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns. , 2001, Journal of neurophysiology.

[27]  W. K. Metcalfe,et al.  Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva , 1986, The Journal of comparative neurology.

[28]  Yen-Hong Kao,et al.  Imaging the Functional Organization of Zebrafish Hindbrain Segments during Escape Behaviors , 1996, Neuron.

[29]  J. Diamond,et al.  Startle-response in Teleost Fish: an Elementary Circuit for Neural Discrimination , 1968, Nature.

[30]  W. K. Metcalfe,et al.  Early axonal contacts during development of an identified dendrite in the brain of the zebrafish , 1990, Neuron.

[31]  C. Kimmel,et al.  Morphogenesis and synaptogenesis of the zebrafish mauthner neuron , 1981, The Journal of comparative neurology.

[32]  Melina E. Hale,et al.  Grading Movement Strength by Changes in Firing Intensity versus Recruitment of Spinal Interneurons , 2007, Neuron.

[33]  Thomas K. Berger,et al.  Combined voltage and calcium epifluorescence imaging in vitro and in vivo reveals subthreshold and suprathreshold dynamics of mouse barrel cortex. , 2007, Journal of neurophysiology.

[34]  Haruko Matsui,et al.  Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behaviour , 1998, Nature.

[35]  J. McKENDRICK,et al.  The Central Nervous System of Vertebrates , 1909, Nature.

[36]  E. Gahtan,et al.  Evidence for a widespread brain stem escape network in larval zebrafish. , 2002, Journal of neurophysiology.

[37]  S. Grillner,et al.  Visual pathways for postural control and negative phototaxis in lamprey. , 1997, Journal of neurophysiology.

[38]  D. Raible,et al.  Ultrastructural analysis of aminoglycoside‐induced hair cell death in the zebrafish lateral line reveals an early mitochondrial response , 2007, The Journal of comparative neurology.

[39]  Henri Korn,et al.  Neurobiology of the Mauthner cell , 1978 .

[40]  Ethan Gahtan,et al.  Visually guided injection of identified reticulospinal neurons in zebrafish: A survey of spinal arborization patterns , 2003, The Journal of comparative neurology.

[41]  M B Foreman,et al.  The direction change concept for reticulospinal control of goldfish escape , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  A. Ménard,et al.  Initiation of locomotion in lampreys , 2008, Brain Research Reviews.

[43]  C. Kimmel,et al.  The development and behavioral characteristics of the startle response in the zebra fish. , 1974, Developmental psychobiology.

[44]  J. T. Hackett,et al.  The behavioral role of the Mauthner neuron impulse , 1986, Behavioral and Brain Sciences.

[45]  H. Korn,et al.  Physiological properties of the mauthner system in the adult zebrafish , 1998, The Journal of comparative neurology.

[46]  R. Farley,et al.  Mauthner neuron field potential in newly hatched larvae of the zebra fish. , 1975, Journal of neurophysiology.

[47]  Robert C. Eaton,et al.  The motor output of the Mauthner cell, a reticulospinal command neuron , 1990, Brain Research.

[48]  J. Fetcho,et al.  In Vivo Imaging of Zebrafish Reveals Differences in the Spinal Networks for Escape and Swimming Movements , 2001, The Journal of Neuroscience.

[49]  S. Zottoli,et al.  Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. , 1977, The Journal of experimental biology.

[50]  Julie A. Harris,et al.  Neomycin-induced Hair Cell Death and Rapid Regeneration in the Lateral Line of Zebrafish (danio Rerio) , 2022 .

[51]  D. O'Malley,et al.  Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. , 2000, The Journal of experimental biology.

[52]  D. Faber,et al.  Otolith endorgan input to the Mauthner neuron in the goldfish , 2007, The Journal of comparative neurology.

[53]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[54]  Shennan A. Weiss,et al.  Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus) , 2006, Journal of Experimental Biology.

[55]  Y. Oda,et al.  Common Sensory Inputs and Differential Excitability of Segmentally Homologous Reticulospinal Neurons in the Hindbrain , 2004, The Journal of Neuroscience.

[56]  J. Fetcho,et al.  Spinal network of the Mauthner cell. , 1991, Brain, behavior and evolution.

[57]  Michael Granato,et al.  Sensorimotor Gating in Larval Zebrafish , 2007, The Journal of Neuroscience.

[58]  Richard R. Fay,et al.  The Auditory Periphery in Fishes , 1999 .

[59]  F. Sasaki,et al.  Internalization of styryl dye FM1-43 in the hair cells of lateral line organs in Xenopus larvae. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[60]  D. Raible,et al.  Developmental differences in susceptibility to neomycin-induced hair cell death in the lateral line neuromasts of zebrafish (Danio rerio) , 2003, Hearing Research.

[61]  Liang Li,et al.  Tactile, acoustic and vestibular systems sum to elicit the startle reflex , 2002, Neuroscience & Biobehavioral Reviews.

[62]  D. C. Winters,et al.  Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus ) , 1999, Journal of Comparative Physiology A.

[63]  Y. Fukami,et al.  EFFECTS OF STRYCHNINE AND PROCAINE ON COLLATERAL INHIBITION OF THE MAUTHNER CELL OF GOLDFISH. , 1964, The Japanese journal of physiology.

[64]  Paul W. Frankland,et al.  The acoustic startle reflex: neurons and connections , 1995, Brain Research Reviews.

[65]  Robert C. Eaton,et al.  Alternative neural pathways initiate fast-start responses following lesions of the mauthner neuron in goldfish , 1982, Journal of comparative physiology.

[66]  R. C. Eaton,et al.  Differential activation of Mauthner and non-Mauthner startle circuits in the zebrafish: Implications for functional substitution , 1984, Journal of Comparative Physiology A.