Skip to main content
Log in

Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Several concepts developed in the nineteenth century have formed the basis of much of our neuroanatomical teaching today. Not all of these were based on solid evidence nor have withstood the test of time. Recent evidence on the evolution and development of the autonomic nervous system, combined with molecular insights into the development and diversification of motor neurons, challenges some of the ideas held for over 100 years about the organization of autonomic motor outflow. This review provides an overview of the original ideas and quality of supporting data and contrasts this with a more accurate and in depth insight provided by studies using modern techniques. Several lines of data demonstrate that branchial motor neurons are a distinct motor neuron population within the vertebrate brainstem, from which parasympathetic visceral motor neurons of the brainstem evolved. The lack of an autonomic nervous system in jawless vertebrates implies that spinal visceral motor neurons evolved out of spinal somatic motor neurons. Consistent with the evolutionary origin of brainstem parasympathetic motor neurons out of branchial motor neurons and spinal sympathetic motor neurons out of spinal motor neurons is the recent revision of the organization of the autonomic nervous system into a cranial parasympathetic and a spinal sympathetic division (e.g., there is no sacral parasympathetic division). We propose a new nomenclature that takes all of these new insights into account and avoids the conceptual misunderstandings and incorrect interpretation of limited and technically inferior data inherent in the old nomenclature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abitua PB, Wagner E, Navarrete IA, Levine M (2012) Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492:104–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abitua PB, Gainous TB, Kaczmarczyk AN, Winchell CJ, Hudson C, Kamata K, Nakagawa M, Tsuda M, Kusakabe TG, Levine M (2015) The pre-vertebrate origins of neurogenic placodes. Nature 524:462–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahlborn F (1884) Ueber den Ursprung und Austritt der Hirnnerven von Petromyzon. Zeit Wiss Zool40:1884

    Google Scholar 

  • Albuixech-Crespo B, López-Blanch L, Burguera D, Maeso I, Sánchez Arrones L, Moreno-Bravo JA, Somorjai I, Pascual-Anaya J, Puelles E, Bovolenta P (2017) Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain. PLoS Biol

  • Balfour FM (1880) A treatise on comparative embryology. Macmillan, London

    Book  Google Scholar 

  • Bell C (1811) Idea of a new anatomy of the brain submitted for the observations of my friends. Strahan and Preston, London

  • Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, Bellen HJ, Fritzsch B, Zoghbi HY (2001) Proprioceptor pathway development is dependent on Math1. Neuron 30:411–422

    Article  CAS  PubMed  Google Scholar 

  • Bosley TM, Oystreck DT, Robertson RL, al Awad A, Abu-Amero K, Engle EC (2006) Neurological features of congenital fibrosis of the extraocular muscles type 2 with mutations in PHOX2A. Brain 129:2363–2374

    Article  PubMed  Google Scholar 

  • Bronner ME, LeDouarin NM (2012) Development and evolution of the neural crest: an overview. Dev Biol 366:2–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346

    CAS  PubMed  Google Scholar 

  • Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Takano-Maruyama M, Gaufo GO (2011) Plasticity of neural crest–placode interaction in the developing visceral nervous system. Dev Dyn 240:1880–1888

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Desai J, Miranda CJ, Duncan JS, Qiu W, Nugent AA, Kolpak AL, Wu CC, Drokhlyansky E, Delisle MM (2014) Human CFEOM1 mutations attenuate KIF21A autoinhibition and cause oculomotor axon stalling. Neuron 82:334–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coppola E, Rallu M, Richard J, Dufour S, Riethmacher D, Guillemot F, Goridis C, Brunet J-F (2010) Epibranchial ganglia orchestrate the development of the cranial neurogenic crest. Proc Natl Acad Sci U S A 107:2066–2071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dasen JS, Liu J-P, Jessell TM (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425:926–933

    Article  CAS  PubMed  Google Scholar 

  • Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477–491

    Article  CAS  PubMed  Google Scholar 

  • Davis-Dusenbery BN, Williams LA, Klim JR, Eggan K (2014) How to make spinal motor neurons. Development 141:491–501

    Article  CAS  PubMed  Google Scholar 

  • Dufour HD, Chettouh Z, Deyts C, De Rosa R, Goridis C, Joly J-S, Brunet J-F (2006) Precraniate origin of cranial motoneurons. Proc Natl Acad Sci U S A 103:8727–8732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyachuk V, Furlan A, Shahidi MK, Giovenco M, Kaukua N, Konstantinidou C, Pachnis V, Memic F, Marklund U, Müller T (2014) Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345:82–87

    Article  CAS  PubMed  Google Scholar 

  • Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417–1430

    Article  CAS  PubMed  Google Scholar 

  • Edinger L (1885) Über den Verlauf der centralen Hirnnervenbahnen mit Demonstrationen von Präparaten. Arch Psychiat Nervenkr 16:858–859

    Google Scholar 

  • Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, Van Heyningen V, Jessell T, Briscoe J (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90:169–180

    Article  CAS  PubMed  Google Scholar 

  • Espinosa-Medina I, Outin E, Picard C, Chettouh Z, Dymecki S, Consalez G, Coppola E, Brunet J-F (2014) Parasympathetic ganglia derive from Schwann cell precursors. Science 345:87–90

    Article  CAS  PubMed  Google Scholar 

  • Espinosa-Medina I, Saha O, Boismoreau F, Chettouh Z, Rossi F, Richardson W, Brunet J-F (2016) The sacral autonomic outflow is sympathetic. Science 354:893–897

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B (1998) Of mice and genes: evolution of vertebrate brain development. Brain Behav Evol 52:207–217

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Glover J (2006) Evolution of the Deuterostome central nervous system: an intercalation of developmental patterning processes with cellular specification processes-2.01

  • Fritzsch B, Northcutt RG (1993a) Cranial and spinal nerve organization in amphioxus and lampreys: evidence for an ancestral craniate pattern. Cells Tissues Organs 148:96–109

    Article  CAS  Google Scholar 

  • Fritzsch B, Northcutt RG (1993b) Origin and migration of trochlear, oculomotor and abducent motor neurons in Petromyzon Marinus L. Dev Brain Res 74:122–126

    Article  CAS  Google Scholar 

  • Fritzsch B, Sonntag R, Dubuc R, Ohta Y, Grillner S (1990) Organization of the six motor nuclei innervating the ocular muscles in lamprey. J Comp Neurol 294:491–506

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Christensen M, Nichols D (1993) Fiber pathways and positional changes in efferent perikarya of 2.5-to 7-day chick embryos as revealed with dil and dextran amiens. J Neurobiol 24:1481–1499

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Nichols D, Echelard Y, McMahon A (1995) Development of midbrain and anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice. J Neurobiol 27:457–469

    Article  CAS  PubMed  Google Scholar 

  • Gaskell W (1880) On the tonicity of the heart and blood vessels. J Physiol 3:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaskell WH (1886) On the structure, distribution and function of the nerves which innervate the visceral and vascular systems. J Physiol 7:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaskell WH (1889) On the relation between the structure, function, distribution and origin of the cranial nerves; together with a theory of the origin of the nervous system of vertebrata. J Physiol 10:153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaskell WH (1908) The origin of vertebrates. Longmans Green, Harlow

    Book  Google Scholar 

  • Gaskell WH (1920) The involuntary nervous system. Longmans Green, Harlow

    Google Scholar 

  • Gilland E, Baker R (1993) Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Cells Tissues Organs 148:110–123

    Article  CAS  Google Scholar 

  • Glasco DM, Pike W, Qu Y, Reustle L, Misra K, Di Bonito M, Studer M, Fritzsch B, Goffinet AM, Tissir F (2016) The atypical cadherin Celsr 1 functions non-cell autonomously to block rostral migration of facial branchiomotor neurons in mice. Dev Biol 417:40–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glover JC (1991) Inductive events in the neural tube. Trends Neurosci 14:424–427

    Article  CAS  PubMed  Google Scholar 

  • Glover JC (2001) Correlated patterns of neuron differentiation and Hox gene expression in the hindbrain: a comparative analysis. Brain Res Bull 55:683–693

    Article  CAS  PubMed  Google Scholar 

  • Glover JC (2003) The development of vestibulo-ocular circuitry in the chicken embryo. J Physiol 97:17–25

    Google Scholar 

  • Golden MG, Dasen JS (2012) Polycomb repressive complex 1 activities determine the columnar organization of motor neurons. Genes Dev 26:2236–2250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haines DE (2004) Neuroanatomy: an atlas of structures, sections, and systems. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Häming D, Simoes-Costa M, Uy B, Valencia J, Sauka-Spengler T, Bronner-Fraser M (2011) Expression of sympathetic nervous system genes in lamprey suggests their recruitment for specification of a new vertebrate feature. PloS ONE 6:e26543

    Article  PubMed  PubMed Central  Google Scholar 

  • Heaton MB, Moody SA (1980) Early development and migration of the trigeminal motor nucleus in the chick embryo. J Comp Neurol 189:61–99

    Article  CAS  PubMed  Google Scholar 

  • Herrick CJ (1918) An introduction to neurology. Saunders, New South Wales

    Google Scholar 

  • Herrick CJ (1922) An introduction to neurology. Saunders, New South Wales

    Google Scholar 

  • Herrick CJ (1948) The brain of the tiger salamander. Ambystoma tigrinum. University of Chicago Press, Chicago

  • Hinckley CA, Alaynick WA, Gallarda BW, Hayashi M, Hilde KL, Driscoll SP, Dekker JD, Tucker HO, Sharpee TO, Pfaff SL (2015) Spinal locomotor circuits develop using hierarchical rules based on motorneuron position and identity. Neuron 87:1008–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirsch M-R, Glover JC, Dufour HD, Brunet J-F, Goridis C (2007) Forced expression of Phox 2 homeodomain transcription factors induces a branchio-visceromotor axonal phenotype. Dev Biol 303:687–702

    Article  CAS  PubMed  Google Scholar 

  • His W (1889) Die Neuroblasten und deren Entstehung im embryonalen Mark. S. Hirzel

  • Ju M, Aroca P, Luo J, Puelles L, Redies C (2004) Molecular profiling indicates avian branchiomotor nuclei invade the hindbrain alar plate. Neuroscience 128:785–796

    Article  CAS  PubMed  Google Scholar 

  • Jung H, Dasen JS (2015) Evolution of patterning systems and circuit elements for locomotion. Dev Cell 32:408–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, de Caprona D, Fritzsch B (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429:615–630

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Fontelonga T, Roesener AP, Lee H, Gurung S, Mendonca PR, Mastick GS (2015a) Motor neuron cell bodies are actively positioned by slit/Robo repulsion and Netrin/DCC attraction. Dev Biol 399:68–79

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Fontelonga T, Roesener AP, Lee H, Gurung S, Mendonca PRF, Mastick GS (2015b) Motor neuron cell bodies are actively positioned by slit/Robo repulsion and Netrin/DCC attraction. Dev Biol 399:68–79

    Article  CAS  PubMed  Google Scholar 

  • Langley J (1900) The sympathetic and other related systems of nerves. Textbook of physiology 2:616–696

    Google Scholar 

  • Langley JN (1905) On the reaction of cells and of nerve-endings to certain poisons, chiefly as regards the reaction of striated muscle to nicotine and to curari. J Physiol 33:374

    Article  PubMed  PubMed Central  Google Scholar 

  • Langley JN (1921) The autonomic nervous system (pt. I)

  • Levi-Montalcini R (1964) Events in the developing nervous system. Prog Brain Res 4:1–29

    Article  Google Scholar 

  • Levi-Montalcini R (1997) The origin and development of the visceral system in the spinal. The saga of the nerve growth factor: preliminary studies, discovery, further development. World Scientific, Singapore

  • Litingtung Y, Chiang C (2000) Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli 3. Nat Neurosci 3:979–985

    Article  CAS  PubMed  Google Scholar 

  • Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J (2015) The deuterostome context of chordate origins. Nature 520:456–465

    Article  CAS  PubMed  Google Scholar 

  • Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75–86

    Article  CAS  PubMed  Google Scholar 

  • Lumsden A, Keynes R (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424–428

    Article  CAS  PubMed  Google Scholar 

  • Machado TA, Pnevmatikakis E, Paninski L, Jessell TM, Miri A (2015) Primacy of flexor locomotor pattern revealed by ancestral reversion of motor neuron identity. Cell 162:338–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marín F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738

    Article  PubMed  Google Scholar 

  • Marín F, Aroca P, Puelles L (2008) Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230–247

    Article  PubMed  Google Scholar 

  • Markham JA, Vaughn JE. (1991) Migration patterns of sympathetic preganglionic neurons in embryonic rat spinal cord. J Neurobiol. 22(8):811-22

  • Müller M, Jabs N, Lork DE, Fritzsch B, Sander M (2003) Nkx 6. 1 controls migration and axon pathfinding of cranial branchio-motoneurons. Development 130:5815–5826

    Article  PubMed  Google Scholar 

  • Murakami Y, Pasqualetti M, Takio Y, Hirano S, Rijli FM, Kuratani S (2004) Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131:983–995

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys R, Puelles L (2016) The fundamental morphological units (FMUs) of the CNS. Towards a new Neuromorphology. Springer, Berlin, pp 143–196

    Google Scholar 

  • Nieuwenhuys R, ten Donkelaar H, Nicholson С (1998) The central nervous system of vertebrates. vol 1. Springer, Berlin

  • Nijssen J, Comley LH, Hedlund E (2017) Motor neuron vulnerability and resistance in amyotrophic lateral sclerosis. Acta Neuropathol:1–23

  • Nilsson S (2011) Comparative anatomy of the autonomic nervous system. Auton Neurosci 165:3–9

    Article  PubMed  Google Scholar 

  • Nomaksteinsky M, Kassabov S, Chettouh Z, Stoeklé H-C, Bonnaud L, Fortin G, Kandel ER, Brunet J-F (2013) Ancient origin of somatic and visceral neurons. BMC Biol 11:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Oh S, Huang X, Liu J, Litingtung Y, Chiang C (2009) Shh and Gli 3 activities are required for timely generation of motor neuron progenitors. Dev Biol 331:261–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker HJ, Bronner ME, Krumlauf R (2014) A Hox regulatory network of hindbrain segmentation is conserved to the base of vertebrates. Nature 514:490–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker HJ, Bronner ME, Krumlauf R (2016) The vertebrate Hox gene regulatory network for hindbrain segmentation: evolution and diversification. BioEssays 38:526–538

    Article  CAS  PubMed  Google Scholar 

  • Pasini A, Manenti R, Rothbacher U, Lemaire P (2012) Antagonizing retinoic acid and FGF/MAPK pathways control posterior body patterning in the invertebrate chordate Ciona intestinalis. PLoS ONE 7:e46193

  • Pattyn A, Morin X, Cremer H, Goridis C, Brunet J-F (1997) Expression and interactions of the two closely related homeobox genes Phox 2a and Phox 2b during neurogenesis. Development 124:4065–4075

    CAS  PubMed  Google Scholar 

  • Pattyn A, Morin X, Cremer H, Goridis C, Brunet J-F (1999) The homeobox gene Phox 2b is essential for the development of autonomic neural crest derivatives. Nature 399:366–370

    Article  CAS  PubMed  Google Scholar 

  • Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl 1 in motor neuron generation reveals a motor neuron–dependent step in interneuron differentiation. Cell 84:309–320

    Article  CAS  PubMed  Google Scholar 

  • Puelles L, Privat A (1977) Do oculomotor neuroblasts migrate across the midline in the fetal rat brain? Anat Embryol 150:187–206

    Article  CAS  PubMed  Google Scholar 

  • Romer AS (1970) The vertebrate body. WB saunders, Philadelphia

    Google Scholar 

  • Romer AS (1972) The vertebrate as a dual animal—somatic and visceral. Evolutionary biology. Springer, Berlin, pp 121-156

  • Sander M, Paydar S, Ericson J, Briscoe J, Berber E, German M, Jessell TM, Rubenstein JL (2000) Ventral neural patterning by Nkx homeobox genes: Nkx 6. 1 controls somatic motor neuron and ventral interneuron fates. Genes Dev 14:2134–2139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoenwolf GC, Alvarez IS (1991) Specification of neurepithelium and surface epithelium in avian transplantation chimeras. Development 112:713–722

    CAS  PubMed  Google Scholar 

  • Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F (2015) Hemichordate genomes and deuterostome origins. Nature

  • Simmons D, Duncan J, de Caprona DC, Fritzsch B (2011) Development of the inner ear efferent system. Auditory and vestibular efferents. Springer, Berlin, pp 187–216

    Book  Google Scholar 

  • SØviknes AM, Chourrout D, Glover JC (2007) Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura Dioica. J Comp Neurol 503:224–243

    Article  PubMed  Google Scholar 

  • Sternfeld, Matthew J., Christopher A. Hinckley, Niall J. Moore, Matthew T. Pankratz, Kathryn L. Hilde, Shawn P. Driscoll, Marito Hayashi et al. Speed and segmentation control mechanisms characterized in rhythmically-active circuits created from spinal neurons produced from genetically-tagged embryonic stem cells. eLife; 6:e21540

  • Tiveron M-C, Pattyn A, Hirsch M-R, Brunet J-F (2003) Role of Phox 2b and mash 1 in the generation of the vestibular efferent nucleus. Dev Biol 260:46–57

    Article  CAS  PubMed  Google Scholar 

  • Tomás-Roca L, Corral-San-Miguel R, Aroca P, Puelles L, Marín F (2016) Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features. Brain Struct Funct 221:815–838

    Article  PubMed  Google Scholar 

  • Tsuchida T, Ensini M, Morton S, Baldassare M, Edlund T, Jessell T, Pfaff S (1994) Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79:957–970

    Article  CAS  PubMed  Google Scholar 

  • Watson C, Shimogori T, Puelles L (2017) Mouse Fgf 8-Cre-Lac Z lineage analysis defines the territory of the postnatal mammalian isthmus. J Comp Neurol

  • Williams PL, Warwick R, Dyson M, Bannister LH (1989) Gray’s anatomy. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Windle WF, Austin MF (1936) Neurofibeillar development in the central nervous system of chick embryos up to 5 days’ incubation. J Comp Neurol 63:431–463

    Article  Google Scholar 

  • Winslow J-B (1732) Exposition anatomique de la structure du corps humain par Jacques Bénigne Winslow. Chez G. Desprez et J. Desessartz

  • Wygoda JA, Yang Y, Byrne M, Wray GA (2014) Transcriptomic analysis of the highly derived radial body plan of a sea urchin. Genome biology and evolution 6:964–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada T, Placzek M, Tanaka H, Dodd J, Jessell T (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64:635–647

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61–73

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We express our gratitude to Dr. J-F Brunet for critically reviewing an earlier version and adding valuable comments to improve the manuscript. We also appreciate the helpful comments and susggestions prvided by an unknown reviewer. This work was supported by NIH (RO1 DC005590 to BF; R03 DC013655 to IJ; R03 DC015333 to KE).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bernd Fritzsch.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fritzsch, B., Elliott, K.L. & Glover, J.C. Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature. Cell Tissue Res 370, 195–209 (2017). https://doi.org/10.1007/s00441-017-2676-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-017-2676-y

Keywords

Navigation