FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Neurosci / Characterization of Dmrt3-Derived Neurons Suggest a Role wit...
The Journal of neuroscience : the official journal of the Society for Neuroscience2018; 39(10); 1771-1782; doi: 10.1523/JNEUROSCI.0326-18.2018

Characterization of Dmrt3-Derived Neurons Suggest a Role within Locomotor Circuits.

Abstract: Neuronal networks within the spinal cord, collectively known as the central pattern generator (CPG), coordinate rhythmic movements underlying locomotion. The transcription factor doublesex and mab-3-related transcription factor 3 (DMRT3) is involved in the differentiation of the dorsal interneuron 6 class of spinal cord interneurons. In horses, a non-sense mutation in the gene has major effects on gaiting ability, whereas mice lacking the gene display impaired locomotor activity. Although the gene is necessary for normal spinal network formation and function in mice, a direct role for -derived neurons in locomotor-related activities has not been demonstrated. Here we present the characteristics of the -derived spinal cord interneurons. Using transgenic mice of both sexes, we characterized interneurons labeled by their expression of Cre driven by the endogenous promoter. We used molecular, retrograde tracing and electrophysiological techniques to examine the anatomical, morphological, and electrical properties of the Dmrt3-Cre neurons. We demonstrate that inhibitory Dmrt3-Cre neurons receive extensive synaptic inputs, innervate surrounding CPG neurons, intrinsically regulate CPG neuron's electrical activity, and are rhythmically active during fictive locomotion, bursting at frequencies independent to the ventral root output. The present study provides novel insights on the character of spinal -derived neurons, data demonstrating that these neurons participate in locomotor coordination. In this work, we provide evidence for a role of the Dmrt3 interneurons in spinal cord locomotor circuits as well as molecular and functional insights on the cellular and microcircuit level of the Dmrt3-expressing neurons in the spinal cord. Dmrt3 neurons provide the first example of an interneuron population displaying different oscillation frequencies. This study presents novel findings on an under-reported population of spinal cord neurons, which will aid in deciphering the locomotor network and will facilitate the design and development of therapeutics for spinal cord injury and motor disorders.
Copyright © 2019 the authors 0270-6474/19/391771-12$15.00/0.
Get Full Text
Publication Date: 2018-12-21 PubMed ID: 30578339PubMed Central: PMC6407301DOI: 10.1523/JNEUROSCI.0326-18.2018Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research discusses how Dmrt3-derived spinal cord interneurons function within locomotor circuits, meaning they play a key role in coordinating rhythmic bodily movements, like walking. The study also reveals that these neurons participate in and contribute significantly to overall locomotor coordination.

Central Pattern Generator (CPG) and DMRT3

  • The central pattern generator (CPG) is a network of neurons in the spinal cord that are responsible for rhythmic movements underlying locomotion.
  • DMRT3 (doublesex and mab-3-related transcription factor 3) is a transcription factor involved in the differentiation of a class of spinal cord interneurons, commonly referred to as the dorsal interneuron.
  • Mutations in the DMRT3 gene have been linked to significant effects on gaiting ability in horses and impaired locomotor activity in mice, indicating its crucial role in normal spinal network formation and function.

Role of Dmrt3-Derived Neurons in Locomotor Circuits

  • The study demonstrates for the first time a direct role for Dmrt3-derived neurons in locomotor-related activities.
  • Using a combination of molecular, retrograde tracing, and electrophysiological techniques, the research outlines the anatomical, morphological, and electrical properties of the Dmrt3-Cre neurons.
  • The results showed that Dmrt3-Cre neurons receive extensive synaptic inputs, directly innervate surrounding CPG neurons, regulate CPG neuron’s electrical activity, and are active during fictive locomotion with frequencies independently regulated from the ventral root output.
  • The individuality of oscillation frequencies displayed by these neurons is a novel and significant finding.

Importance of this Research

  • These discoveries provide a deeper understanding of the role of Dmrt3 interneurons in spinal cord locomotor circuits.
  • This knowledge can be used to further our understanding of the locomotor network and can play an important role in the development of treatments for spinal cord injuries and motor disorders.

Cite This Article

APA
Perry S, Larhammar M, Vieillard J, Nagaraja C, Hilscher MM, Tafreshiha A, Rofo F, Caixeta FV, Kullander K. (2018). Characterization of Dmrt3-Derived Neurons Suggest a Role within Locomotor Circuits. J Neurosci, 39(10), 1771-1782. https://doi.org/10.1523/JNEUROSCI.0326-18.2018

Publication

The Journal of neuroscience : the official journal of the Society for Neuroscience
ISSN: 1529-2401
NlmUniqueID: 8102140
Country: United States
Language: English
Volume: 39
Issue: 10
Pages: 1771-1782

Researcher Affiliations

Perry, Sharn
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Larhammar, Martin
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden klas.kullander@neuro.uu.se martin.larhammar@gmail.com.
Vieillard, Jennifer
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Nagaraja, Chetan
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Hilscher, Markus M
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Tafreshiha, Atieh
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Rofo, Fadi
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Caixeta, Fabio V
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden.
Kullander, Klas
  • Department of Neuroscience, Uppsala University, 751 24 Uppsala, Sweden klas.kullander@neuro.uu.se martin.larhammar@gmail.com.

MeSH Terms

  • Animals
  • Central Pattern Generators
  • Female
  • Gene Knock-In Techniques
  • Interneurons / cytology
  • Interneurons / physiology
  • Locomotion
  • Male
  • Membrane Potentials
  • Mice, Inbred C57BL
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Spinal Cord / cytology
  • Spinal Cord / physiology
  • Transcription Factors / physiology

References

This article includes 50 references
  1. Adibi M, McDonald JS, Clifford CW, Arabzadeh E. Adaptation improves neural coding efficiency despite increasing correlations in variability.. J Neurosci 2013 Jan 30;33(5):2108-20.
    doi: 10.1523/JNEUROSCI.3449-12.2013pmc: PMC6619115pubmed: 23365247google scholar: lookup
  2. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, Pennacchio LA, Rubin EM. Deletion of ultraconserved elements yields viable mice.. PLoS Biol 2007 Sep;5(9):e234.
    doi: 10.1371/journal.pbio.0050234pmc: PMC1964772pubmed: 17803355google scholar: lookup
  3. Alvarez FJ, Villalba RM, Zerda R, Schneider SP. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses.. J Comp Neurol 2004 May 3;472(3):257-80.
    doi: 10.1002/cne.20012pubmed: 15065123google scholar: lookup
  4. Andersson LS, Larhammar M, Memic F, Wootz H, Schwochow D, Rubin CJ, Patra K, Arnason T, Wellbring L, Hjälm G, Imsland F, Petersen JL, McCue ME, Mickelson JR, Cothran G, Ahituv N, Roepstorff L, Mikko S, Vallstedt A, Lindgren G, Andersson L, Kullander K. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice.. Nature 2012 Aug 30;488(7413):642-6.
    doi: 10.1038/nature11399pmc: PMC3523687pubmed: 22932389google scholar: lookup
  5. Borowska J, Jones CT, Zhang H, Blacklaws J, Goulding M, Zhang Y. Functional subpopulations of V3 interneurons in the mature mouse spinal cord.. J Neurosci 2013 Nov 20;33(47):18553-65.
    doi: 10.1523/jneurosci.2005-13.2013pmc: PMC3894417pubmed: 24259577google scholar: lookup
  6. Butt SJ, Harris-Warrick RM, Kiehn O. Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator.. J Neurosci 2002 Nov 15;22(22):9961-71.
    doi: 10.1523/jneurosci.22-22-09961.2002pmc: PMC6757818pubmed: 12427853google scholar: lookup
  7. Dougherty KJ, Kiehn O. Functional organization of V2a-related locomotor circuits in the rodent spinal cord.. Ann N Y Acad Sci 2010 Jun;1198:85-93.
    doi: 10.1111/j.1749-6632.2010.05502.xpubmed: 20536923google scholar: lookup
  8. Dumoulin A, Rostaing P, Bedet C, Lévi S, Isambert MF, Henry JP, Triller A, Gasnier B. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons.. J Cell Sci 1999 Mar;112 ( Pt 6):811-23.
    pubmed: 10036231doi: 10.1242/jcs.112.6.811google scholar: lookup
  9. Dyck J, Lanuza GM, Gosgnach S. Functional characterization of dI6 interneurons in the neonatal mouse spinal cord.. J Neurophysiol 2012 Jun;107(12):3256-66.
    doi: 10.1152/jn.01132.2011pmc: PMC3378412pubmed: 22442567google scholar: lookup
  10. Eide AL, Glover J, Kjaerulff O, Kiehn O. Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord.. J Comp Neurol 1999 Jan 18;403(3):332-45.
    doi: 10.1002/(SICI)1096-9861(19990118)403:3<332::AID-CNE4>3.0.CO;2-Rpubmed: 9886034google scholar: lookup
  11. Enjin A, Rabe N, Nakanishi ST, Vallstedt A, Gezelius H, Memic F, Lind M, Hjalt T, Tourtellotte WG, Bruder C, Eichele G, Whelan PJ, Kullander K. Identification of novel spinal cholinergic genetic subtypes disclose Chodl and Pitx2 as markers for fast motor neurons and partition cells.. J Comp Neurol 2010 Jun 15;518(12):2284-304.
    doi: 10.1002/cne.22332pubmed: 20437528google scholar: lookup
  12. Göbel W, Helmchen F. In vivo calcium imaging of neural network function.. Physiology (Bethesda) 2007 Dec;22:358-65.
    doi: 10.1152/physiol.00032.2007pubmed: 18073408google scholar: lookup
  13. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction.. Nat Rev Neurosci 2009 Jul;10(7):507-18.
    doi: 10.1038/nrn2608pmc: PMC2847453pubmed: 19543221google scholar: lookup
  14. Griener A, Zhang W, Kao H, Haque F, Gosgnach S. Anatomical and electrophysiological characterization of a population of dI6 interneurons in the neonatal mouse spinal cord.. Neuroscience 2017 Oct 24;362:47-59.
    doi: 10.1016/j.neuroscience.2017.08.031pubmed: 28844009google scholar: lookup
  15. Grillner S. Locomotion in vertebrates: central mechanisms and reflex interaction.. Physiol Rev 1975 Apr;55(2):247-304.
    doi: 10.1152/physrev.1975.55.2.247pubmed: 1144530google scholar: lookup
  16. Haddad GG, Getting PA. Repetitive firing properties of neurons in the ventral region of nucleus tractus solitarius. In vitro studies in adult and neonatal rat.. J Neurophysiol 1989 Dec;62(6):1213-24.
    doi: 10.1152/jn.1989.62.6.1213pubmed: 2600620google scholar: lookup
  17. Haque F, Rancic V, Zhang W, Clugston R, Ballanyi K, Gosgnach S. WT1-Expressing Interneurons Regulate Left-Right Alternation during Mammalian Locomotor Activity.. J Neurosci 2018 Jun 20;38(25):5666-5676.
    doi: 10.1523/JNEUROSCI.0328-18.2018pmc: PMC6595980pubmed: 29789381google scholar: lookup
  18. He C, Chen F, Li B, Hu Z. Neurophysiology of HCN channels: from cellular functions to multiple regulations.. Prog Neurobiol 2014 Jan;112:1-23.
    doi: 10.1016/j.pneurobio.2013.10.001pubmed: 24184323google scholar: lookup
  19. Johannssen HC, Helmchen F. Two-photon imaging of spinal cord cellular networks.. Exp Neurol 2013 Apr;242:18-26.
    doi: 10.1016/j.expneurol.2012.07.014pubmed: 22849822google scholar: lookup
  20. Joosten EA, Bär PR, Gispen WH. Collagen implants and cortico-spinal axonal growth after mid-thoracic spinal cord lesion in the adult rat.. J Neurosci Res 1995 Jul 1;41(4):481-90.
    doi: 10.1002/jnr.490410407pubmed: 7473879google scholar: lookup
  21. Kiehn O, Kjaerulff O, Tresch MC, Harris-Warrick RM. Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord.. Brain Res Bull 2000 Nov 15;53(5):649-59.
    doi: 10.1016/S0361-9230(00)00398-1pubmed: 11165800google scholar: lookup
  22. Kim S, Kettlewell JR, Anderson RC, Bardwell VJ, Zarkower D. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad.. Gene Expr Patterns 2003 Mar;3(1):77-82.
    doi: 10.1016/S1567-133X(02)00071-6pubmed: 12609607google scholar: lookup
  23. Kinnischtzke AK, Sewall AM, Berkepile JM, Fanselow EE. Postnatal maturation of somatostatin-expressing inhibitory cells in the somatosensory cortex of GIN mice.. Front Neural Circuits 2012;6:33.
    doi: 10.3389/fncir.2012.00033pmc: PMC3364579pubmed: 22666189google scholar: lookup
  24. Kjaerulff O, Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study.. J Neurosci 1996 Sep 15;16(18):5777-94.
    doi: 10.1523/JNEUROSCI.16-18-05777.1996pmc: PMC6578971pubmed: 8795632google scholar: lookup
  25. Kjaerulff O, Kiehn O. Crossed rhythmic synaptic input to motoneurons during selective activation of the contralateral spinal locomotor network.. J Neurosci 1997 Dec 15;17(24):9433-47.
    doi: 10.1523/JNEUROSCI.17-24-09433.1997pmc: PMC6573410pubmed: 9390999google scholar: lookup
  26. Kullander K. Genetics moving to neuronal networks.. Trends Neurosci 2005 May;28(5):239-47.
    doi: 10.1016/j.tins.2005.03.001pubmed: 15866198google scholar: lookup
  27. Kwan AC, Dietz SB, Webb WW, Harris-Warrick RM. Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord.. J Neurosci 2009 Sep 16;29(37):11601-13.
    doi: 10.1523/JNEUROSCI.1612-09.2009pmc: PMC2756057pubmed: 19759307google scholar: lookup
  28. Lamotte d'Incamps B, Ascher P. Four excitatory postsynaptic ionotropic receptors coactivated at the motoneuron-Renshaw cell synapse.. J Neurosci 2008 Dec 24;28(52):14121-31.
    doi: 10.1523/JNEUROSCI.3311-08.2008pmc: PMC6671456pubmed: 19109494google scholar: lookup
  29. Langer D, van 't Hoff M, Keller AJ, Nagaraja C, Pfäffli OA, Göldi M, Kasper H, Helmchen F. HelioScan: a software framework for controlling in vivo microscopy setups with high hardware flexibility, functional diversity and extendibility.. J Neurosci Methods 2013 Apr 30;215(1):38-52.
    doi: 10.1016/j.jneumeth.2013.02.006pubmed: 23416135google scholar: lookup
  30. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements.. Neuron 2004 May 13;42(3):375-86.
    doi: 10.1016/S0896-6273(04)00249-1pubmed: 15134635google scholar: lookup
  31. Larhammar M, Patra K, Blunder M, Emilsson L, Peuckert C, Arvidsson E, Rönnlund D, Preobraschenski J, Birgner C, Limbach C, Widengren J, Blom H, Jahn R, Wallén-Mackenzie Å, Kullander K. SLC10A4 is a vesicular amine-associated transporter modulating dopamine homeostasis.. Biol Psychiatry 2015 Mar 15;77(6):526-36.
    doi: 10.1016/j.biopsych.2014.07.017pubmed: 25176177google scholar: lookup
  32. Leao KE, Leao RN, Sun H, Fyffe RE, Walmsley B. Hyperpolarization-activated currents are differentially expressed in mice brainstem auditory nuclei.. J Physiol 2006 Nov 1;576(Pt 3):849-64.
    doi: 10.1113/jphysiol.2006.114702pmc: PMC1890420pubmed: 16916913google scholar: lookup
  33. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain.. Nat Neurosci 2010 Jan;13(1):133-40.
    doi: 10.1038/nn.2467pmc: PMC2840225pubmed: 20023653google scholar: lookup
  34. Meyer M, de Angelis MH, Wurst W, Kühn R. Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases.. Proc Natl Acad Sci U S A 2010 Aug 24;107(34):15022-6.
    doi: 10.1073/pnas.1009424107pmc: PMC2930558pubmed: 20686113google scholar: lookup
  35. Micallef L, Rodgers P. eulerAPE: drawing area-proportional 3-Venn diagrams using ellipses.. PLoS One 2014;9(7):e101717.
    doi: 10.1371/journal.pone.0101717pmc: PMC4102485pubmed: 25032825google scholar: lookup
  36. Mor Y, Lev-Tov A. Analysis of rhythmic patterns produced by spinal neural networks.. J Neurophysiol 2007 Nov;98(5):2807-17.
    doi: 10.1152/jn.00740.2007pubmed: 17715187google scholar: lookup
  37. Pape HC. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons.. Annu Rev Physiol 1996;58:299-327.
    doi: 10.1146/annurev.ph.58.030196.001503pubmed: 8815797google scholar: lookup
  38. Perry S, Gezelius H, Larhammar M, Hilscher MM, Lamotte d'Incamps B, Leao KE, Kullander K. Firing properties of Renshaw cells defined by Chrna2 are modulated by hyperpolarizing and small conductance ion currents Ih and ISK.. Eur J Neurosci 2015 Apr;41(7):889-900.
    doi: 10.1111/ejn.12852pubmed: 25712471google scholar: lookup
  39. Rabe N, Gezelius H, Vallstedt A, Memic F, Kullander K. Netrin-1-dependent spinal interneuron subtypes are required for the formation of left-right alternating locomotor circuitry.. J Neurosci 2009 Dec 16;29(50):15642-9.
    doi: 10.1523/JNEUROSCI.5096-09.2009pmc: PMC6666172pubmed: 20016078google scholar: lookup
  40. Schnerwitzki D, Perry S, Ivanova A, Caixeta FV, Cramer P, Günther S, Weber K, Tafreshiha A, Becker L, Vargas Panesso IL, Klopstock T, Hrabe de Angelis M, Schmidt M, Kullander K, Englert C. Neuron-specific inactivation of Wt1 alters locomotion in mice and changes interneuron composition in the spinal cord.. Life Sci Alliance 2018 Aug;1(4):e201800106.
    doi: 10.26508/lsa.201800106pmc: PMC6238623pubmed: 30456369google scholar: lookup
  41. Smith CA, Hurley TM, McClive PJ, Sinclair AH. Restricted expression of DMRT3 in chicken and mouse embryos.. Mech Dev 2002 Dec;119 Suppl 1:S73-6.
    doi: 10.1016/S0925-4773(03)00094-7pubmed: 14516663google scholar: lookup
  42. Stosiek C, Garaschuk O, Holthoff K, Konnerth A. In vivo two-photon calcium imaging of neuronal networks.. Proc Natl Acad Sci U S A 2003 Jun 10;100(12):7319-24.
    doi: 10.1073/pnas.1232232100pmc: PMC165873pubmed: 12777621google scholar: lookup
  43. Trichas G, Begbie J, Srinivas S. Use of the viral 2A peptide for bicistronic expression in transgenic mice.. BMC Biol 2008 Sep 15;6:40.
    doi: 10.1186/1741-7007-6-40pmc: PMC2553761pubmed: 18793381google scholar: lookup
  44. Vallstedt A, Kullander K. Dorsally derived spinal interneurons in locomotor circuits.. Ann N Y Acad Sci 2013 Mar;1279:32-42.
    doi: 10.1111/j.1749-6632.2012.06801.xpubmed: 23531000google scholar: lookup
  45. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein.. J Neurosci 2005 Jun 15;25(24):5710-9.
    doi: 10.1523/jneurosci.0274-05.2005pmc: PMC6724883pubmed: 15958737google scholar: lookup
  46. Wilson JM, Blagovechtchenski E, Brownstone RM. Genetically defined inhibitory neurons in the mouse spinal cord dorsal horn: a possible source of rhythmic inhibition of motoneurons during fictive locomotion.. J Neurosci 2010 Jan 20;30(3):1137-48.
    doi: 10.1523/JNEUROSCI.1401-09.2010pmc: PMC5061569pubmed: 20089922google scholar: lookup
  47. Wu L, Sonner PM, Titus DJ, Wiesner EP, Alvarez FJ, Ziskind-Conhaim L. Properties of a distinct subpopulation of GABAergic commissural interneurons that are part of the locomotor circuitry in the neonatal spinal cord.. J Neurosci 2011 Mar 30;31(13):4821-33.
    doi: 10.1523/JNEUROSCI.4764-10.2011pmc: PMC3086198pubmed: 21451020google scholar: lookup
  48. Wu X, Liao L, Liu X, Luo F, Yang T, Li C. Is ZD7288 a selective blocker of hyperpolarization-activated cyclic nucleotide-gated channel currents?. Channels (Austin) 2012 Nov-Dec;6(6):438-42.
    doi: 10.4161/chan.22209pmc: PMC3536728pubmed: 22989944google scholar: lookup
  49. Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM, Miles GB. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity.. Neuron 2009 Dec 10;64(5):645-62.
    doi: 10.1016/j.neuron.2009.10.017pmc: PMC2891428pubmed: 20005822google scholar: lookup
  50. Zhong G, Droho S, Crone SA, Dietz S, Kwan AC, Webb WW, Sharma K, Harris-Warrick RM. Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord.. J Neurosci 2010 Jan 6;30(1):170-82.
    doi: 10.1523/JNEUROSCI.4849-09.2010pmc: PMC2824326pubmed: 20053899google scholar: lookup

Citations

This article has been cited 16 times.
  1. Vincelette A. The Characteristics, Distribution, Function, and Origin of Alternative Lateral Horse Gaits.. Animals (Basel) 2023 Aug 8;13(16).
    doi: 10.3390/ani13162557pubmed: 37627349google scholar: lookup
  2. Wilson AC, Sweeney LB. Spinal cords: Symphonies of interneurons across species.. Front Neural Circuits 2023;17:1146449.
    doi: 10.3389/fncir.2023.1146449pubmed: 37180760google scholar: lookup
  3. Gosgnach S. Spinal inhibitory interneurons: regulators of coordination during locomotor activity.. Front Neural Circuits 2023;17:1167836.
    doi: 10.3389/fncir.2023.1167836pubmed: 37151357google scholar: lookup
  4. Vieillard J, Franck MCM, Hartung S, Jakobsson JET, Ceder MM, Welsh RE, Lagerström MC, Kullander K. Adult spinal Dmrt3 neurons receive direct somatosensory inputs from ipsi- and contralateral primary afferents and from brainstem motor nuclei.. J Comp Neurol 2023 Jan;531(1):5-24.
    doi: 10.1002/cne.25405pubmed: 36214727google scholar: lookup
  5. Gupta S, Kawaguchi R, Heinrichs E, Gallardo S, Castellanos S, Mandric I, Novitch BG, Butler SJ. In vitro atlas of dorsal spinal interneurons reveals Wnt signaling as a critical regulator of progenitor expansion.. Cell Rep 2022 Jul 19;40(3):111119.
    doi: 10.1016/j.celrep.2022.111119pubmed: 35858555google scholar: lookup
  6. Xu S, Zhang S, Zhang W, Liu H, Wang M, Zhong L, Bian W, Chen X. Genome-Wide Identification, Phylogeny, and Expression Profile of the Dmrt (Doublesex and Mab-3 Related Transcription Factor) Gene Family in Channel Catfish (Ictalurus punctatus).. Front Genet 2022;13:891204.
    doi: 10.3389/fgene.2022.891204pubmed: 35571040google scholar: lookup
  7. Bernhardt N, Memic F, Velica A, Tran MA, Vieillard J, Sayyab S, Chersa T, Andersson L, Whelan PJ, Boije H, Kullander K. Hop Mice Display Synchronous Hindlimb Locomotion and a Ventrally Fused Lumbar Spinal Cord Caused by a Point Mutation in Ttc26.. eNeuro 2022 Mar-Apr;9(2).
    doi: 10.1523/ENEURO.0518-21.2022pubmed: 35210288google scholar: lookup
  8. Iglesias González AB, Jakobsson JET, Vieillard J, Lagerström MC, Kullander K, Boije H. Single Cell Transcriptomic Analysis of Spinal Dmrt3 Neurons in Zebrafish and Mouse Identifies Distinct Subtypes and Reveal Novel Subpopulations Within the dI6 Domain.. Front Cell Neurosci 2021;15:781197.
    doi: 10.3389/fncel.2021.781197pubmed: 35002627google scholar: lookup
  9. Kikkawa T, Osumi N. Multiple Functions of the Dmrt Genes in the Development of the Central Nervous System.. Front Neurosci 2021;15:789583.
    doi: 10.3389/fnins.2021.789583pubmed: 34955736google scholar: lookup
  10. Sławińska U, Majczyński H, Kwaśniewska A, Miazga K, Cabaj AM, Bekisz M, Jordan LM, Zawadzka M. Unusual Quadrupedal Locomotion in Rat during Recovery from Lumbar Spinal Blockade of 5-HT(7) Receptors.. Int J Mol Sci 2021 Jun 2;22(11).
    doi: 10.3390/ijms22116007pubmed: 34199392google scholar: lookup
  11. Stachowski NJ, Dougherty KJ. Spinal Inhibitory Interneurons: Gatekeepers of Sensorimotor Pathways.. Int J Mol Sci 2021 Mar 6;22(5).
    doi: 10.3390/ijms22052667pubmed: 33800863google scholar: lookup
  12. Carneiro M, Vieillard J, Andrade P, Boucher S, Afonso S, Blanco-Aguiar JA, Santos N, Branco J, Esteves PJ, Ferrand N, Kullander K, Andersson L. A loss-of-function mutation in RORB disrupts saltatorial locomotion in rabbits.. PLoS Genet 2021 Mar;17(3):e1009429.
    doi: 10.1371/journal.pgen.1009429pubmed: 33764968google scholar: lookup
  13. Ho KH, Patrizi A. Assessment of common housekeeping genes as reference for gene expression studies using RT-qPCR in mouse choroid plexus.. Sci Rep 2021 Feb 8;11(1):3278.
    doi: 10.1038/s41598-021-82800-5pubmed: 33558629google scholar: lookup
  14. Uemura Y, Kato K, Kawakami K, Kimura Y, Oda Y, Higashijima SI. Neuronal Circuits That Control Rhythmic Pectoral Fin Movements in Zebrafish.. J Neurosci 2020 Aug 26;40(35):6678-6690.
    doi: 10.1523/JNEUROSCI.1484-20.2020pubmed: 32703904google scholar: lookup
  15. Del Pozo A, Manuel R, Iglesias Gonzalez AB, Koning HK, Habicher J, Zhang H, Allalou A, Kullander K, Boije H. Behavioral Characterization of dmrt3a Mutant Zebrafish Reveals Crucial Aspects of Vertebrate Locomotion through Phenotypes Related to Acceleration.. eNeuro 2020 May Jun;7(3).
    doi: 10.1523/ENEURO.0047-20.2020pubmed: 32357958google scholar: lookup
  16. Haque F, Gosgnach S. Mapping Connectivity Amongst Interneuronal Components of the Locomotor CPG.. Front Cell Neurosci 2019;13:443.
    doi: 10.3389/fncel.2019.00443pubmed: 31636541google scholar: lookup
Subscribe to our newsletter
Join 99,359 horse owners like you who receive our email updates on horse health and nutrition.