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PMID: 18264094 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Control of visually guided behavior by distinct populations of spinal projection neurons.

Nature neuroscience ·Vol. 11 ·No. 3 ·2008-03-00 ·Pages 327-33

Orger MB, Kampff AR, Severi KE, Bollmann JH, Engert F

Abstract

A basic question in the field of motor control is how different actions are represented by activity in spinal projection neurons. We used a new behavioral assay to identify visual stimuli that specifically drive basic motor patterns in zebrafish. These stimuli evoked consistent patterns of neural activity in the neurons projecting to the spinal cord, which we could map throughout the entire population using in vivo two-photon calcium imaging. We found that stimuli that drive distinct behaviors activated distinct subsets of projection neurons, consisting, in some cases, of just a few cells. This stands in contrast to the distributed activation seen for more complex behaviors. Furthermore, targeted cell by cell ablations of the neurons associated with evoked turns abolished the corresponding behavioral response. This description of the functional organization of the zebrafish motor system provides a framework for identifying the complete circuit underlying a vertebrate behavior.

MeSH Terms
Action Potentials/physiology Animals Axons/physiology,ultrastructure Brain Stem/anatomy & histology,physiology Calcium/chemistry Denervation Efferent Pathways/anatomy & histology,physiology Fluorescent Dyes Functional Laterality/physiology Indicators and Reagents Locomotion/physiology Models, Animal Nerve Net/cytology,physiology Neurons/cytology,physiology Orientation/physiology Psychomotor Performance/physiology Reticular Formation/anatomy & histology,physiology Spinal Cord/anatomy & histology,physiology Staining and Labeling Swimming/physiology Visual Pathways/physiology Zebrafish/anatomy & histology,physiology
Chemicals
Fluorescent Dyes Indicators and Reagents Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Orger Michael B
Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA. morger@mcb.harvard.edu
Kampff Adam R
Severi Kristen E
Bollmann Johann H
Engert Florian
References (44)
44 references, click to expand
  1. Encoding and decoding of reticulospinal commands.
    Brain Res Brain Res Rev. 2002 Oct;40(1-3):166-77 PMID: 12589915
  2. Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish.
    J Neurosci. 2007 May 16;27(20):5271-9 PMID: 17507550
  3. Neuronal activity during different behaviors in Aplysia: a distributed organization?
    Science. 1994 Feb 11;263(5148):820-3 PMID: 8303300
  4. Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture.
    J Exp Biol. 2000 Sep;203(Pt 17):2565-79 PMID: 10934000
  5. The motor output of the Mauthner cell, a reticulospinal command neuron.
    Brain Res. 1990 May 28;517(1-2):88-98 PMID: 2376010
  6. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish.
    Neuron. 1999 Jun;23(2):325-35 PMID: 10399938
  7. Fos-like immunohistochemical identification of neurons active during the startle response of the rainbow trout.
    J Comp Neurol. 2001 Oct 22;439(3):306-14 PMID: 11596056
  8. The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation.
    BMC Neurosci. 2006 Apr 06;7:30 PMID: 16600041
  9. The Mauthner cell half a century later: a neurobiological model for decision-making?
    Neuron. 2005 Jul 7;47(1):13-28 PMID: 15996545
  10. Dynamic sensorimotor interactions in locomotion.
    Physiol Rev. 2006 Jan;86(1):89-154 PMID: 16371596
  11. Perception of Fourier and non-Fourier motion by larval zebrafish.
    Nat Neurosci. 2000 Nov;3(11):1128-33 PMID: 11036270
  12. Identifiable reticulospinal neurons of the adult zebrafish, Brachydanio rerio.
    J Comp Neurol. 1991 Feb 1;304(1):34-52 PMID: 2016411
  13. Interaction between hindbrain and spinal networks during the development of locomotion in zebrafish.
    Dev Neurobiol. 2007 Jun;67(7):933-47 PMID: 17506502
  14. Directionally selective calcium signals in dendrites of starburst amacrine cells.
    Nature. 2002 Aug 22;418(6900):845-52 PMID: 12192402
  15. Development of reticulospinal neurons of the zebrafish. II. Early axonal outgrowth and cell body position.
    J Comp Neurol. 1986 Sep 8;251(2):172-84 PMID: 3782497
  16. Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus).
    J Comp Physiol A. 1999 Feb;184(2):207-18 PMID: 10192953
  17. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits.
    J Neurosci. 2006 May 24;26(21):5684-97 PMID: 16723525
  18. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum.
    J Neurosci. 2005 Oct 5;25(40):9294-303 PMID: 16207889
  19. Brain neurons which project to the spinal cord in young larvae of the zebrafish.
    J Comp Neurol. 1982 Feb 20;205(2):112-27 PMID: 7076887
  20. Rapid lesioning of large numbers of identified vertebrate neurons: applications in zebrafish.
    J Neurosci Methods. 2001 Jul 15;108(1):97-110 PMID: 11459623
  21. Two-photon laser scanning fluorescence microscopy.
    Science. 1990 Apr 6;248(4951):73-6 PMID: 2321027
  22. Prey capture by larval zebrafish: evidence for fine axial motor control.
    Brain Behav Evol. 2002;60(4):207-29 PMID: 12457080
  23. A topographic map of recruitment in spinal cord.
    Nature. 2007 Mar 1;446(7131):71-5 PMID: 17330042
  24. Of lasers, mutants, and see-through brains: functional neuroanatomy in zebrafish.
    J Neurobiol. 2004 Apr;59(1):147-61 PMID: 15007833
  25. Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva.
    J Comp Neurol. 1986 Sep 8;251(2):147-59 PMID: 3782495
  26. Grading movement strength by changes in firing intensity versus recruitment of spinal interneurons.
    Neuron. 2007 Jan 4;53(1):91-102 PMID: 17196533
  27. Combinations of muscle synergies in the construction of a natural motor behavior.
    Nat Neurosci. 2003 Mar;6(3):300-8 PMID: 12563264
  28. Common principles of motor control in vertebrates and invertebrates.
    Annu Rev Neurosci. 1993;16:265-97 PMID: 8460894
  29. Sensorimotor gating in larval zebrafish.
    J Neurosci. 2007 May 2;27(18):4984-94 PMID: 17475807
  30. Modulation of locomotor activity in larval zebrafish during light adaptation.
    J Exp Biol. 2007 Jul;210(Pt 14):2526-39 PMID: 17601957
  31. Time course of the development of motor behaviors in the zebrafish embryo.
    J Neurobiol. 1998 Dec;37(4):622-32 PMID: 9858263
  32. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate.
    Development. 1999 Sep;126(17):3757-67 PMID: 10433906
  33. INTERNEURONS COMMANDING SWIMMERET MOVEMENTS IN THE CRAYFISH, PROCAMBARUS CLARKI (GIRARD).
    Comp Biochem Physiol. 1964 Aug;12:509-25 PMID: 14206963
  34. Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey.
    Eur J Neurosci. 2005 Nov;22(9):2271-82 PMID: 16262665
  35. Modular organization of spinal motor systems.
    Neuroscientist. 2002 Oct;8(5):437-42 PMID: 12374428
  36. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum.
    Neuron. 2005 Mar 24;45(6):941-51 PMID: 15797554
  37. Visually guided injection of identified reticulospinal neurons in zebrafish: a survey of spinal arborization patterns.
    J Comp Neurol. 2003 Apr 28;459(2):186-200 PMID: 12640669
  38. Evidence for a widespread brain stem escape network in larval zebrafish.
    J Neurophysiol. 2002 Jan;87(1):608-14 PMID: 11784774
  39. Imaging the functional organization of zebrafish hindbrain segments during escape behaviors.
    Neuron. 1996 Dec;17(6):1145-55 PMID: 8982162
  40. Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator.
    J Neurophysiol. 2003 Dec;90(6):3986-97 PMID: 12930818
  41. Optical imaging of neuronal populations during decision-making.
    Science. 2005 Feb 11;307(5711):896-901 PMID: 15705844
  42. Mechanisms of pulsed laser ablation of biological tissues.
    Chem Rev. 2003 Feb;103(2):577-644 PMID: 12580643
  43. Sensory-motor transformation by individual command neurons.
    J Neurosci. 2007 Jan 31;27(5):1024-32 PMID: 17267556
  44. Ensemble coding of vocal control in birdsong.
    J Neurosci. 2005 Jan 19;25(3):652-61 PMID: 15659602
Article Info
Journal
Nature neuroscience
Abbr.
Nat Neurosci
ISSN
1097-6256
DOI
10.1038/nn2048
Email
morger@mcb.harvard.edu
Published
2008-03-00
Epub
2008-00-10
Pages
327-33
Language
English
Region
United States
NLM ID
9809671
PMCID
PMC2894808
Subset
IM
Grants
NEI NIH HHS · R01 EY014429 · United States
NEI NIH HHS · R01 EY014429-05 · United States
NEI NIH HHS · R01 EY014429-01A2 · United States
Corrections
CommentIn
PMID: 18301430
External Links
PubMed source DOI: 10.1038/nn2048 PMC Full Text View journal details
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