Imaging the Functional Organization of Zebrafish Hindbrain Segments during Escape Behaviors

Although vertebrate hindbrains are segmented structures, the functional significance of the segmentation is unknown. In zebrafish, the hindbrain segments contain serially repeated classes of individually identifiable neurons. We took advantage of the transparency of larval zebrafish and used confocal calcium imaging in the intact fish to study the activity of one set of individually identified, serially homologous reticulospinal cells (the Mauthner cell, MID2cm, and MID3cm) during behavior. Behavioral studies predicted that differential activity in this set of serially homologous neurons might serve to control the directionality of the escape behavior that fish use to avoid predators. We found that the serially homologous cells are indeed activated during escapes and that the combination of cells activated depends upon the location of the sensory stimulus used to elicit the escape. The patterns of activation we observed were exactly those predicted by behavioral studies. The data suggest that duplication of ancestral hindbrain segments, and subsequent functional diversification, resulted in sets of related neurons whose activity patterns create behavioral variability.

[1]  Arie E. Kaufman,et al.  Visualization of calcium activity in nerve cells , 1995, IEEE Computer Graphics and Applications.

[2]  P. Adams,et al.  Subcellular calcium transients visualized by confocal microscopy in a voltage-clamped vertebrate neuron. , 1990, Science.

[3]  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.

[4]  W. K. Metcalfe,et al.  Brain neurons which project to the spinal cord in young larvae of the zebrafish , 1982, The Journal of comparative neurology.

[5]  Michael J. O'Donovan,et al.  Real-time imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes , 1993, Journal of Neuroscience Methods.

[6]  R. Keynes,et al.  Segmental patterns of neuronal development in the chick hindbrain , 1989, Nature.

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

[8]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

[9]  A. Schier,et al.  Zebrafish: genetic tools for studying vertebrate development. , 1994, Trends in genetics : TIG.

[10]  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.

[11]  J. Fetcho,et al.  Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Remo Guidieri Res , 1995, RES: Anthropology and Aesthetics.

[13]  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.

[14]  H. Chiel,et al.  Neural architectures for adaptive behavior , 1994, Trends in Neurosciences.

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

[16]  W. N. Ross,et al.  Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. , 1992, Journal of neurophysiology.

[17]  C. Kimmel,et al.  Organization of hindbrain segments in the zebrafish embryo , 1990, Neuron.

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

[19]  C. Nüsslein-Volhard,et al.  Mutational approaches to studying embryonic pattern formation in the zebrafish. , 1993, Current opinion in genetics & development.

[20]  M. Westerfield,et al.  Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. , 1988, Development.

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

[22]  W. Cruce,et al.  Evolution of Motor Systems: The Reticulospinal Pathways , 1984 .

[23]  D. Tank,et al.  Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation , 1989, Nature.

[24]  D. O'Malley Calcium permeability of the neuronal nuclear envelope: evaluation using confocal volumes and intracellular perfusion , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  J. Fetcho,et al.  Visualization of active neural circuitry in the spinal cord of intact zebrafish. , 1995, Journal of neurophysiology.

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

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

[28]  S. Fraser,et al.  Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions , 1990, Nature.

[29]  J. Rubenstein,et al.  The embryonic vertebrate forebrain: the prosomeric model. , 1994, Science.

[30]  F. Krasne,et al.  The organization of escape behaviour in the crayfish. , 1972, The Journal of experimental biology.

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

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

[33]  Michael J. O'Donovan,et al.  Combined retrograde labeling and calcium imaging in spinal cord and brainstem neurons of the lamprey , 1994, Brain Research.

[34]  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.

[35]  D. Featherstone,et al.  Short Communication: Noninvasive Detection of Electrical Events During the Startle Response in Larval Medaka , 1991 .

[36]  D. Faber,et al.  Neuronal Networks Underlying the Escape Response in Goldfish , 1989, Annals of the New York Academy of Sciences.