Cited by 82Neurotransmitter Receptor Influence on BehaviorZebrafish Biomedical Research ApplicationsNeuroscience and Neuropharmacology Research

Firing dynamics and modulatory actions of supraspinal dopaminergic neurons during zebrafish locomotor behavior

Open access
Jay, Michael, De Faveri, Francesca, McDearmid, Jonathan Robert·2015·Current Biology

Abstract

BACKGROUND: Dopamine (DA) has long been known to have modulatory effects on vertebrate motor circuits. However, the types of information encoded by supraspinal DAergic neurons and their relationship to motor behavior remain unknown. RESULTS: By conducting electrophysiological recordings from awake, paralyzed zebrafish larvae that can produce behaviorally relevant activity patterns, we show that supraspinal DAergic neurons generate two forms of output: tonic spiking and phasic bursting. Using paired supraspinal DA neuron and motoneuron recordings, we further show that these firing modes are associated with specific behavioral states. Tonic spiking is prevalent during periods of inactivity while bursting strongly correlates with locomotor output. Targeted laser ablation of supraspinal DA neurons reduces motor episode frequency without affecting basic parameters of motor output, strongly suggesting that these cells regulate spinal network excitability. CONCLUSIONS: Our findings reveal how vertebrate motor circuit flexibility is temporally controlled by supraspinal DAergic pathways and provide important insights into the functional significance of this evolutionarily conserved cell population.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.cub.2014.12.033

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Paired recordings of diencephalospinal dopaminergic neurons and spinal MNs during swimming show that these two populations often burst together.

    “Paired recordings of diencephalospinal dopaminergic neurons and spinal MNs during swimming show that these two populations often burst together (Jay et al., 2015).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Jay et al., 2015

    In Results, ‘Relationship between DDN Activity and Motor Behavior’ (page unavailable), the paper reports simultaneous recordings of DDNs and spinal motoneurons or muscle fibers; 43 of 45 DDN bursts occurred during the beat component of fictive swimming. It describes the spinal recording as rhythmic synaptic drive, however, rather than showing that motoneurons themselves burst alongside DDNs. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 41

  1. [1]Garraway S.M. Hochman S. Modulatory actions of serotonin, norepinephrine, dopamine, and acetylcholine in spinal cord deep dorsal horn neurons J. Neurophysiol. 86 2001 2183 2194 11698510
  2. [2]Clemens S. Hochman S. Conversion of the modulatory actions of dopamine on spinal reflexes from depression to facilitation in D3 receptor knock-out mice J. Neurosci. 24 2004 11337 11345 15601940 PMC2731231
  3. [3]Gladwell S.J. Coote J.H. Inhibitory and indirect excitatory effects of dopamine on sympathetic preganglionic neurones in the neonatal rat spinal cord in vitro Brain Res. 818 1999 397 407 10082825
  4. [4]Schotland J. Shupliakov O. Wikström M. Brodin L. Srinivasan M. You Z.B. Herrera-Marschitz M. Zhang W. Hökfelt T. Grillner S. Control of lamprey locomotor neurons by colocalized monoamine transmitters Nature 374 1995 266 268 7885446
  5. [5]Han P. Nakanishi S.T. Tran M.A. Whelan P.J. Dopaminergic modulation of spinal neuronal excitability J. Neurosci. 27 2007 13192 13204 18045913 PMC6673410
  6. [6]Clemens S. Belin-Rauscent A. Simmers J. Combes D. Opposing modulatory effects of D1- and D2-like receptor activation on a spinal central pattern generator J. Neurophysiol. 107 2012 2250 2259 22262823
  7. [7]Kiehn O. Kjaerulff O. Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat J. Neurophysiol. 75 1996 1472 1482 8727391
  8. [8]Thirumalai V. Cline H.T. Endogenous dopamine suppresses initiation of swimming in prefeeding zebrafish larvae J. Neurophysiol. 100 2008 1635 1648 18562547 PMC2544474
  9. [9]Barrière G. Mellen N. Cazalets J.R. Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat Eur. J. Neurosci. 19 2004 1325 1335 15016090
  10. [10]Gordon I.T. Whelan P.J. Monoaminergic control of cauda-equina-evoked locomotion in the neonatal mouse spinal cord J. Neurophysiol. 96 2006 3122 3129 16956991
  11. [11]Humphreys J.M. Whelan P.J. Dopamine exerts activation-dependent modulation of spinal locomotor circuits in the neonatal mouse J. Neurophysiol. 108 2012 3370 3381 22993259
  12. [12]Christie K.J. Whelan P.J. Monoaminergic establishment of rostrocaudal gradients of rhythmicity in the neonatal mouse spinal cord J. Neurophysiol. 94 2005 1554 1564 15829596
  13. [14]Reimer M.M. Norris A. Ohnmacht J. Patani R. Zhong Z. Dias T.B. Kuscha V. Scott A.L. Chen Y.C. Rozov S. Dopamine from the brain promotes spinal motor neuron generation during development and adult regeneration Dev. Cell 25 2013 478 491 23707737
  14. [15]Tay T.L. Ronneberger O. Ryu S. Nitschke R. Driever W. Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems Nat. Commun. 2 2011 171 21266970 PMC3105308
  15. [16]Rink E. Wullimann M.F. The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum) Brain Res. 889 2001 316 330 11166725
  16. [17]Rink E. Wullimann M.F. Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study Brain Res. Dev. Brain Res. 137 2002 89 100 12128258
  17. [18]Ryu S. Mahler J. Acampora D. Holzschuh J. Erhardt S. Omodei D. Simeone A. Driever W. Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development Curr. Biol. 17 2007 873 880 17481897
  18. [19]Wen L. Wei W. Gu W. Huang P. Ren X. Zhang Z. Zhu Z. Lin S. Zhang B. Visualization of monoaminergic neurons and neurotoxicity of MPTP in live transgenic zebrafish Dev. Biol. 314 2008 84 92 18164283
  19. [20]McLean D.L. Fetcho J.R. Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish J. Comp. Neurol. 480 2004 38 56 15515022
  20. [21]Liss B. Roeper J. Ion channels and regulation of dopamine neuron activity Iverson L. Iverson S. Dunnett S. Bjorklund A. Dopamine Handbook 2009 Oxford University Press 118 138
  21. [22]Buss R.R. Drapeau P. Synaptic drive to motoneurons during fictive swimming in the developing zebrafish J. Neurophysiol. 86 2001 197 210 11431502
  22. [23]Hyland B.I. Reynolds J.N.J. Hay J. Perk C.G. Miller R. Firing modes of midbrain dopamine cells in the freely moving rat Neuroscience 114 2002 475 492 12204216
  23. [24]Schultz W. Predictive reward signal of dopamine neurons J. Neurophysiol. 80 1998 1 27 9658025
  24. [25]Paladini C.A. Roeper J. Generating bursts (and pauses) in the dopamine midbrain neurons Neuroscience 282C 2014 109 121 25073045
  25. [26]Lobb C.J. Wilson C.J. Paladini C.A. High-frequency, short-latency disinhibition bursting of midbrain dopaminergic neurons J. Neurophysiol. 105 2011 2501 2511 21367999 PMC3094190
  26. [27]Lobb C.J. Wilson C.J. Paladini C.A. A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons J. Neurophysiol. 104 2010 403 413 20445035 PMC2904231
  27. [28]Deister C.A. Teagarden M.A. Wilson C.J. Paladini C.A. An intrinsic neuronal oscillator underlies dopaminergic neuron bursting J. Neurosci. 29 2009 15888 15897 20016105 PMC2824818
  28. [29]Ryczko D. Grätsch S. Auclair F. Dubé C. Bergeron S. Alpert M.H. Cone J.J. Roitman M.F. Alford S. Dubuc R. Forebrain dopamine neurons project down to a brainstem region controlling locomotion Proc. Natl. Acad. Sci. USA 110 2013 E3235 E3242 23918379 PMC3752272
  29. [30]Fernandes A.M. Beddows E. Filippi A. Driever W. Orthopedia transcription factor otpa and otpb paralogous genes function during dopaminergic and neuroendocrine cell specification in larval zebrafish PLoS ONE 8 2013 e75002 24073233 PMC3779234
  30. [31]Dreyer J.K. Herrik K.F. Berg R.W. Hounsgaard J.D. Influence of phasic and tonic dopamine release on receptor activation J. Neurosci. 30 2010 14273 14283 20962248 PMC6634758
  31. [32]Han P. Whelan P.J. Modulation of AMPA currents by D(1)-like but not D(2)-like receptors in spinal motoneurons Neuroscience 158 2009 1699 1707 19110039
  32. [33]Lapointe N.P. Guertin P.A. Synergistic effects of D1/5 and 5-HT1A/7 receptor agonists on locomotor movement induction in complete spinal cord-transected mice J. Neurophysiol. 100 2008 160 168 18480366
  33. [34]Lapointe N.P. Rouleau P. Ung R.V. Guertin P.A. Specific role of dopamine D1 receptors in spinal network activation and rhythmic movement induction in vertebrates J. Physiol. 587 2009 1499 1511 19204052 PMC2678221
  34. [35]Tsai H.C. Zhang F. Adamantidis A. Stuber G.D. Bonci A. de Lecea L. Deisseroth K. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning Science 324 2009 1080 1084 19389999 PMC5262197
  35. [36]Zweifel L.S. Parker J.G. Lobb C.J. Rainwater A. Wall V.Z. Fadok J.P. Darvas M. Kim M.J. Mizumori S.J. Paladini C.A. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior Proc. Natl. Acad. Sci. USA 106 2009 7281 7288 19342487 PMC2678650
  36. [37]Miyasaka N. Arganda-Carreras I. Wakisaka N. Masuda M. Sümbül U. Seung H.S. Yoshihara Y. Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling Nat. Commun. 5 2014 3639 24714622
  37. [39]Prober D.A. Rihel J. Onah A.A. Sung R.J. Schier A.F. Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish J. Neurosci. 26 2006 13400 13410 17182791 PMC6675014
  38. [40]Kaslin J. Nystedt J.M. Ostergård M. Peitsaro N. Panula P. The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems J. Neurosci. 24 2004 2678 2689 15028760 PMC6729510
  39. [41]Feitl K.E. Ngo V. McHenry M.J. Are fish less responsive to a flow stimulus when swimming? J. Exp. Biol. 213 2010 3131 3137 20802114
  40. [42]Flock A. Russell I.J. The post-synaptic action of efferent fibres in the lateral line organ of the burbot Lota lota J. Physiol. 235 1973 591 605 4772401 PMC1350782
  41. [44]Westerfield M. The Zebrafish Book: A Guide to the Laboratory Use of the Zebrafish (Brachydanio rerio), 2.1 Edition 1994 University of Oregon Press

Cited by

Sorted by citations

Authors
Jay, M., De Faveri, F., & McDearmid, J. R.
Affiliations
University of Leicester (GB)
Corresponding author
McDearmid, Jonathan Robert
Venue
Current Biology
Publisher
Elsevier BV
Published
2015-02
Volume
25
Issue
4
Pages
435-444
ISSN
0960-9822 (ISSN-L)
OpenAlex
W1988448671
Cited by
82
References
2
Citations by year
2026: 4 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 6 · 2021: 14 · 2020: 15 · 2019: 4 · 2018: 7 · 2017: 11 · 2016: 4 · 2015: 4
FWCI
4.04
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Leicester Research Archive (University of Leicester) (submittedVersion, cc-by)
Funders
Biotechnology and Biological Sciences Research Council (1068275, BBE015352)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
dopamine, zebrafish larvae, locomotor behavior, tonic spiking, motor neurons, laser ablation, behavioral state
MeSH terms
Animals, Diencephalon, Locomotion, Motor Neurons, Zebrafish, Dopaminergic Neurons

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review