The Mauthner cell and other identified neurons of the brainstem escape network of fish

This paper reviews the development of our research on the motor consequences of Mauthner cell function and related brainstem neurons. These cells activate fast-start responses such as seen in fishes escaping from predatory attacks. Our goal was to devise a neuroethological theory of fish escape that accurately reconciled the underlying neural function with a correct concept of the motor act. The identified neuron concept of invertebrates greatly influenced the initial studies. Horseradish peroxidase technology allowed us and other workers to identify principal neurons in the brainstem escape system. Digital imaging technology permitted adequate kinematic characterization of the behavior. Resulting experiments showed that Mauthner system demonstrates two general principles of motor organization: (1) the Mauthner cell is a command-like higher order neuron that serially outputs to a lower level central pattern generator; and (2) the Mauthner cell participates in a larger parallel, brainstem escape network. In this network, we showed that the spatio-temporal pattern of activity codes the timing and magnitude of agonist and antagonist trunk muscle contractions during the behavior. Because the approach angle of the stimulus determines these parameters, we were able to discover the overall sensorimotor relationship between stimulus angle and motor output. This relationship is given as a set of descriptive equations written in terms of stimulus angle, magnitude and timing variables of trunk muscle contractions, and resulting escape trajectory. The equations unify the apparent variability of C-start movement patterns into a single, quantitative theory. Recent studies by other workers show how this concept can make accurate predictions about the underlying neural processes, even at the level of the single, identified cell.

[1]  島津 浩,et al.  Vestibular and brain stem control of eye, head and body movements , 1992 .

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

[3]  S. Sharma,et al.  Descending projection neurons to the spinal cord of the goldfish, Carassius auratus , 1987, The Journal of comparative neurology.

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

[5]  S. Rossignol,et al.  Neural Control of Rhythmic Movements in Vertebrates , 1988 .

[6]  R. Calabrese Oscillation in motor pattern-generating networks , 1995, Current Opinion in Neurobiology.

[7]  R. C. Eaton,et al.  Command and the neural causation of behavior: a theoretical analysis of the necessity and sufficiency paradigm. , 1985, Brain, behavior and evolution.

[8]  Robert C. Eaton,et al.  Neural Mechanisms of Startle Behavior , 1984 .

[9]  R. Vertes,et al.  Brainstem mechanisms of behavior , 1990 .

[10]  Olaf Breidbach,et al.  The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach , 1995, Experientia Supplementum.

[11]  M. K. Rock Functional properties of Mauthner cell in the tadpole Rana catesbeiana. , 1980, Journal of neurophysiology.

[12]  P. Webb Effect of Body Form and Response Threshold on the Vulnerability of Four Species of Teleost Prey Attacked by Largemouth Bass (Micropterus salmoides) , 1986 .

[13]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[14]  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.

[15]  R. C. Eaton Eshkol-Wachman movement notation and the evolution of locomotor patterns in vertebrates , 1992, Behavioral and Brain Sciences.

[16]  R. C. Eaton,et al.  Segmental arrangement of reticulospinal neurons in the goldfish hindbrain , 1993, The Journal of comparative neurology.

[17]  E. Seyfarth,et al.  Ludwig Mauthner (1840-1894): neuroanatomist and noted ophthalmologist in Fin-de-Siècle Vienna. , 1991, Brain, behavior and evolution.

[18]  C. A. Brandly,et al.  Advances in Veterinary Science and Comparative Medicine , 1983 .

[19]  U. Will Amphibian Mauthner cells. , 1991, Brain, behavior and evolution.

[20]  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.

[21]  T H BULLOCK Problems in invertebrate electrophysiology. , 1947, Physiological reviews.

[22]  R C Eaton,et al.  Beating the competition: the reliability hypothesis for Mauthner axon size. , 1995, Brain, behavior and evolution.

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

[24]  A. Berthoz,et al.  Relationship between task-related discharge patterns and axonal morphology of brainstem projection neurons involved in orienting eye and head movements , 1992 .

[25]  Robert C. Eaton,et al.  Reticulospinal Control of Rapid Escape Turning Maneuvers in Fishes , 1989 .

[26]  J. Clarke,et al.  Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. , 1993, Development.

[27]  Robert C. Eaton,et al.  The Role of the Mauthner Cell in Fast-Starts Involving Escape in Teleost Fishes , 1984 .

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

[29]  Barry W Peterson,et al.  2 – The Reticulospinal System and Its Role in the Control of Movement , 1984 .

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

[31]  J. C. Fentress Simpler networks and behavior , 1976 .

[32]  R. C. Eaton,et al.  The command neuron concept: Good in theory, difficult to justify in practice , 1986, Behavioral and Brain Sciences.

[33]  A. Björklund Analysis of neuronal microcircuits and synaptic interactions , 1990 .

[34]  K. Pearson Common principles of motor control in vertebrates and invertebrates. , 1993, Annual review of neuroscience.

[35]  T. Finger,et al.  GABAergic innervation of the Mauthner cell and other reticulospinal neurons in the goldfish , 1993, The Journal of comparative neurology.

[36]  R. C. Eaton,et al.  Seven principles for command and the neural causation of behavior. , 1988, Brain, behavior and evolution.

[37]  D L Meyer,et al.  The Mauthner-initiated startle response in teleost fish. , 1977, The Journal of experimental biology.

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

[39]  A. Popper,et al.  The octavolateralis system and Mauthner cell: interactions and questions. , 1995, Brain, behavior and evolution.

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

[41]  R. C. Eaton,et al.  Mauthner and reticulospinal responses to the onset of acoustic pressure and acceleration stimuli. , 1999, Journal of neurophysiology.

[42]  Henri Korn,et al.  Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. , 1991, Brain, behavior and evolution.

[43]  J. Diamond The Mauthner Cell , 1971 .

[44]  K R Svoboda,et al.  Interactions between the neural networks for escape and swimming in goldfish , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  K. R. Weiss,et al.  The command neuron concept , 1978, Behavioral and Brain Sciences.

[46]  S. Guthrie The status of the neural segment , 1995, Trends in Neurosciences.

[47]  E Friauf,et al.  Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  C. Wiersma,et al.  INTERNEURONS COMMANDING SWIMMERET MOVEMENTS IN THE CRAYFISH, PROCAMBARUS CLARKI (GIRARD). , 1964, Comparative biochemistry and physiology.

[49]  James L. Larimer,et al.  Command Fibres in the Circumoesophageal Connectives of Crayfish , 1974 .

[50]  C. R. Fourtner,et al.  Flight Activity Initiated via Giant Interneurons of the Cockroach: Evidence for Bifunctional Trigger Interneurons , 1980, Science.

[51]  C. Kimmel,et al.  Patterning the brain of the zebrafish embryo. , 1993, Annual review of neuroscience.

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

[53]  J Nissanov,et al.  Role of the Mauthner cell in sensorimotor integration by the brain stem escape network. , 1991, Brain, behavior and evolution.

[54]  W. Bollenbacher,et al.  Developmental expression of the prothoracicotropic hormone in the CNS of the Tobacco Hornworm Manduca sexta , 1993, The Journal of comparative neurology.

[55]  J. T. Hackett,et al.  Does the Mauthner cell conform to the criteria of the command neuron concept? , 1981, Brain Research.

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

[57]  P. Webb Exercise performance of fish. , 1994, Advances in veterinary science and comparative medicine.

[58]  A. Stefanelli The Mauthnerian Apparatus in the Ichthyopsida; Its Nature and Function and Correlated Problems of Neurohistogenesis , 1951, The Quarterly Review of Biology.

[59]  Thomas A. Sebeok,et al.  How Animals Communicate , 1979 .

[60]  R. C. Eaton,et al.  How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. , 1991, The Journal of experimental biology.