Skip to main content
Log in

From hindbrain segmentation to breathing after birth

Developmental patterning in rhombomeres 3 and 4

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Respiration is a rhythmic motor behavior that appears in the fetus and acquires a vital importance at birth. It is generated within central pattern-generating neuronal networks of the hindbrain. This region of the brain is of particular interest since it is the most understood part with respect to the cellular and molecular mechanisms that underlie its development. Hox paralogs and Hox-regulating genes kreisler/mafB and Krox20 are required for the normal formation of rhombomeres in vertebrate embryos. From studies of rhombomeres r3 and r4, the authors review mechanisms whereby these developmental genes may govern the early embryonic development of para-facial neuronal networks and specify patterns of motor activities operating throughout life. A model whereby the regional identity of progenitor cells can be abnormally specified in r3 and r4 after a mutation of these genes is proposed. Novel neuronal circuits may develop from some of these misspecified progenitors while others are eliminated, eventually affecting respiration and survival after birth.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Lumsden T. L. (1923) Observation on the respiratory centres in the cat. J. Physiol. 57, 153–160.

    PubMed  CAS  Google Scholar 

  2. Harper R. M., Kinney H. C., Fleming P. J., and Thach B. T. (2000) Sleep influences on homeostatic functions: implications for sudden infant death syndrome. Respir. Physiol. 119(2–3), 123–132.

    PubMed  CAS  Google Scholar 

  3. Kobayashi S., Nishimura M., Yamamoto M., Akiyama Y., Kishi F., and Kawakami Y. (1993) Dyspnea sensation and chemical control of breathing in adult twins. Am. Rev. Respir. Dis. 139, 1192–1198.

    Google Scholar 

  4. Redline S. R. and Tishler P. V. (2000) The genetics of sleep apnea. Sleep Med. Rev. 4, 583–602.

    PubMed  Google Scholar 

  5. Tankersley C. G., Fitzgerald R. S., Levitt R. C., Mitzner W. A., Ewart S. L., and Kleeberger S. R. (1997) Genetic control of differential baseline breathing pattern. J. Appl. Physiol. 82, 874–881.

    PubMed  CAS  Google Scholar 

  6. Mortola J. P. (1987) Dynamics of breathing in newborn mammals. Physiol. Rev. 67, 187–234.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  8. Lumsden A. (1990) The cellular basis of segmentation in the developing hindbrain. TINS 13, 329–335.

    PubMed  CAS  Google Scholar 

  9. Lumsden A. and Krumlauf R. (1996) Patterning the vertebrate neuraxis. Science 274, 1109–1115.

    PubMed  CAS  Google Scholar 

  10. Rijli F. M., Gavalas A., and Chambon P. (1998) Segmentation and specification in the branchial region of the head: the role of the Hox selector genes. Int. J. Dev. Biol. 42, 393–401.

    PubMed  CAS  Google Scholar 

  11. Dupe V., Davenne M., Brocard J., Dolle P., Mark M., Dierich A., Chambon P., and Rijli F. M. (1997) In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′RARE). Development 124(2), 399–410.

    PubMed  CAS  Google Scholar 

  12. Studer M., Gavalas A., Marshall H., Ariza-McNaughton L., Rijli F. M., Chambon P., and Krumlauf R. (1998) Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025–1036.

    PubMed  CAS  Google Scholar 

  13. Gavalas A. and Krumlauf R. (2000) Retinoid signalling and hindbrain patterning. Curr. Opin. Genet. Dev. 10(4), 380–386.

    PubMed  CAS  Google Scholar 

  14. Graham A., Maden M., and Krumlauf R. (1991). The murine Hox-2 genes display dynamic dorsoventral patterns of expression during central nervous system development. Development 112(1), 255–264.

    PubMed  CAS  Google Scholar 

  15. Tiret L., Le Mouellic H., Maury M., and Brulet P. (1998) Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8 deficient mice. Development 125, 279–291.

    PubMed  CAS  Google Scholar 

  16. Davenne M., Maconochie M. K., Neun R., Pattyn A., Chambon P., Krumlauf R., and Rijli F. M. (1999) Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22, 677–691.

    PubMed  CAS  Google Scholar 

  17. Gaufo G. O., Flodby P., and Capecchi M. R. (2000) Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127, 5343–5354.

    PubMed  CAS  Google Scholar 

  18. Mark M., Lufkin T., Vonesh J. L., et al. (1993) Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119, 319–338.

    PubMed  CAS  Google Scholar 

  19. Carpenter E. M., Goddard J. M., Chisaka O., Manley N. R., and Capecchi M. R. (1993) Loss of Hoxa1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063–1075.

    PubMed  CAS  Google Scholar 

  20. Studer M., Lumsden A., Ariza-McNaughton L., Bradley A., and Krumlauf R. (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630–634.

    PubMed  CAS  Google Scholar 

  21. Goddard J. M., Rossel M., Manley N. R., and Capecchi M. R. (1996) Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217–3228.

    PubMed  CAS  Google Scholar 

  22. Barrow J. R. and Capecchi M. R. (1996) Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122(12), 3817–3828.

    PubMed  CAS  Google Scholar 

  23. Gavalas A., Davenne M., Lumsden A., Chambon P., and Rijli F. M. (1997) Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3683–3691.

    Google Scholar 

  24. Gavalas A., Studer M., Lumsden A., Rijli F. M., Krumlauf R., and Chambon P. (1998) Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125, 1123–1136.

    PubMed  CAS  Google Scholar 

  25. Helmbacher F., Pujades C., Desmarquet C., Frain M., Rijli F. M., Chambon P., and Charnay P. (1998) Hoxa1 and Krox-20 synergize to control the development of rhombomere 3. Development 125, 4739–4748.

    PubMed  CAS  Google Scholar 

  26. Rossel M. and Capecchi M. R. (1999) Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development 126, 5027–5040.

    PubMed  CAS  Google Scholar 

  27. Jungbluth S., Bell E., and Lumsden A. (1999) Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development 126, 2751–2758.

    PubMed  CAS  Google Scholar 

  28. Bell E., Wingate R. J., and Lumsden A. (1999) Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284, 2168–2171.

    PubMed  CAS  Google Scholar 

  29. Barrow J. R., Stadler H. S., and Capecchi M. R. (2000) Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 127(5), 933–944.

    PubMed  CAS  Google Scholar 

  30. Pasqualetti M., Neun R., Davenne M., and Rijli F. M. (2001) Retinoic acid rescues inner ear defects in Hoxa1 deficient mice. Nat Genet. 29(1), 34–39.

    PubMed  CAS  Google Scholar 

  31. Pasqualetti M. and Rijli F. M. (2001) Homeobox gene mutations and brain-stem developmental disorders: learning from knockout mice. Curr Opin Neurol. 14(2), 177–184.

    PubMed  CAS  Google Scholar 

  32. Pattyn A., Vallstedt A., Dias J. M., Samad O. A., Krumlauf R., Rijli F. M., Brunet J. F., and Ericson J. (2003) Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes Dev. 17(6), 729–737.

    PubMed  CAS  Google Scholar 

  33. Maves L., Jackman W., and Kimmel C. B. (2002) FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129, 3825–3837.

    PubMed  CAS  Google Scholar 

  34. Walshe J., Maroon H., McGonnell IM., Dickson C., and Mason I. (2002) Establishment of hindbrain segmental identity requires signaling by FGF3 and FGF8. Curr. Biol. 12, 1117–1123.

    PubMed  CAS  Google Scholar 

  35. Marin F. and Charnay P. (2000) Hindbrain patterning: FGFs regulate Krox20 and mafB/kr expression in the otic/preotic region. Development 127, 4925–4935.

    PubMed  CAS  Google Scholar 

  36. Waskiewicz A. J., Rikhof H. A., and Moens C. B. (2002) Eliminating zebrafish PBX proteins reveals a hindbrain ground state. Dev. Cell 3, 723–733.

    PubMed  CAS  Google Scholar 

  37. Hertwig P. (1942) Sechs neue Mutationen bei der Hausmaus in ihrer Bedeutung für allgemeine Vererbungsfragen. YX. Menschl. Vererbgslehre 26, 1–21.

    Google Scholar 

  38. Hertwig P. (1944) Die Genese der Hirn- und Gehörorganmißbildungen bei röntgenmutierten Kreisler-Maüsen. Zeit. Konstlehre 28, 327–354.

    Google Scholar 

  39. Deol M. S. (1964) The abnormalities of the inner ear in kreilser mice. J. Embryol. Exp. Morphol. 12, 475–490.

    PubMed  CAS  Google Scholar 

  40. Manzanares M., Cordes S., Kwan C. T., Sham M. H., Barsh G. S., and Krumlauf R. (1997) Segmental regulation of Hoxb3 by kreisler. Nature 387, 191–195.

    PubMed  CAS  Google Scholar 

  41. Manzanares M., Cordes S., Ariza-McNaughton L., Sadl V., Maruthainar K., Barsh G. S., and Krumlauf R. (1999) Conserved and distinct roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 726(4), 759–769.

    Google Scholar 

  42. Wilkinson D. G., Bhatt S., Chavrier P., Bravo R., and Charnay P. (1989) Segment-specific expression of a zinc finger gene in the developing nervous system of the mouse. Nature 337, 461–464.

    PubMed  CAS  Google Scholar 

  43. Sham M. H., Vesque C., Nonchev S., et al. (1993) The zinc finger gene Krox20 regulates Hoxb-2 (Hox 2.8) during hindbrain segmentation. Cell 72(2), 183–196.

    PubMed  CAS  Google Scholar 

  44. Nonchev S., Maconochie M., Vesque C., et al. (1996) The conserved role of Krox20 in directing Hox gene expression during vertebrate hindbrain segmentation. Proc. Natl. Acad. Sci. USA 93(18), 9339–9345.

    PubMed  CAS  Google Scholar 

  45. Giudicelli F., Taillebourg E., Charnay P., and Gilardi-Hebenstreit P. (2001) Krox20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms. Genes Dev. 15(5), 567–580.

    PubMed  CAS  Google Scholar 

  46. Schneider-Maunoury S., Topilko P., Seitandou T., et al. (1993) Disruption of Krox20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75(6), 1199–1214.

    PubMed  CAS  Google Scholar 

  47. Schneider-Maunoury S., Seitanidou T., Charnay P., and Lumsden A. (1997) Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215–1226.

    PubMed  CAS  Google Scholar 

  48. Swiatek P. J. and Gridley T. (1993) Perinatal lethality and defects in hindbrain development in Krox20 −/− mice for a targeted mutation of the zinc finger gene Krox20. Genes Dev. 7(11), 2071–2084.

    PubMed  CAS  Google Scholar 

  49. Rovainen C. M. (1996) Feeding and breathing in lampreys. Brain Behav. Evol. 48(5), 297–305.

    PubMed  CAS  Google Scholar 

  50. Wild J. M. (1993) The avian nucleus retroambigualis: a nucleus for breathing, singing and calling. Brain Res. 606, 319–324.

    PubMed  CAS  Google Scholar 

  51. Pack A. I. (1993) In: Respiratory Control (Speck, D. F., Dekin, M. S., Revelette, W. R. and Frazier, D. T., eds). Univ. Press of Kentucky, Lexington, pp. 52–57.

    Google Scholar 

  52. McLean H. A., Perry S. F., and Remmers J. E. (1995) Two regions in the isolated brainstem of the frog that modulate respiratory-related activity. J. Comp. Physiol. 177(2), 135–144.

    CAS  Google Scholar 

  53. Wilson R. J., Vasilakos K., Harris M. B., Straus C., and Remmers J. E. (2002) Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators. J. Physiol. 540(2), 557–570.

    PubMed  CAS  Google Scholar 

  54. Takeda R., Remmers J. E., Baker J. P., and Farber J. P. (1986) Postsynaptic potentials of bulbar respiratory neurons of the turtle. Respir. Physiol. 64, 149–160.

    PubMed  CAS  Google Scholar 

  55. Fortin G., Foutz A. S., and Champagnat J. (1994) Respiratory rhythm generation in chick hindbrain: effects of MK-801 and vagotomy. NeuroReport 5(9), 1137–1140.

    PubMed  CAS  Google Scholar 

  56. Milsom W. K. (1991) Intermittent breathing in vertebrates. Annu. Rev. Physiol. 53, 87–105.

    PubMed  CAS  Google Scholar 

  57. Perry S. F., Wilson R. J., Straus C., Harris M. B., and Remmers J. E. (2001) Which came first, the lung or the breath? Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 129(1), 37–47.

    PubMed  CAS  Google Scholar 

  58. Bianchi A. L., Denavit-Saubié M., and Champagnat J. (1995) Central control of breathing in mammals: neuronal circuitry, membrane properties and neurotransmitters. Physiol. Rev. 75, 1–45.

    PubMed  CAS  Google Scholar 

  59. Richter D. W. and Spyer K. M. (2001) Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci. 24(8), 464–472.

    PubMed  CAS  Google Scholar 

  60. Suzue T. (1984) Respiratory rhythm generation in the in vitro brainstem-spinal cord preparation of the neonatal rat. J. Physiol. 354, 173–183.

    PubMed  CAS  Google Scholar 

  61. Smith J. C., Ellenberger H. H., Ballanyi K., Richter D. W., and Feldman J. L. (1991) Pre-Bötzinger complex: a region that may generate respiratory rhythm in mammals. Science 254, 726–729.

    PubMed  CAS  Google Scholar 

  62. Di Pasquale E., Monteau R., and Hilaire G. (1992) In vitro study of central respiratory-like activity of the fetal rat. Exp. Brain Res. 89, 459–464.

    PubMed  Google Scholar 

  63. Onimaru H. and Homma I. (1987) Respiratory rhythm generator neurons in medulla of brainstem-spinal cord preparation from newborn rat. Brain Res. 403(2), 380–384.

    PubMed  CAS  Google Scholar 

  64. Gray P. A., Rekling J. C., Bocchiaro C. M., and Feldman J. L. (1999) Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex. Science 286, 1566–1568.

    PubMed  CAS  Google Scholar 

  65. Lieske S. P., Thoby-Brisson M., Telgkmap P., and Ramirez J. M. (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat. Neurosci. 3(6), 600–607.

    PubMed  CAS  Google Scholar 

  66. Borday V., Kato F., and Champagnat J. (1997) A ventral pontine pathway promotes rhythmic activity in the medulla of neonate mice. NeuroReport 8, 3679–3683.

    PubMed  CAS  Google Scholar 

  67. Onimaru H. and Homma I. (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci. 23(4), 1478–1486.

    PubMed  CAS  Google Scholar 

  68. Denavit-Saubie M., Champagnat J., and Zieglgansberger W. (1978) Effects of opiates and methionine-enkephalin on pontine and bulbar respiratory neurones of the cat. Brain Res. 155(1), 55–67.

    PubMed  CAS  Google Scholar 

  69. Morin-Surun M.-P., Boudinot E., Gacel G., Champagnat J., Roques B. P., and Denavit-Saubie M. (1984) Different effects of mu and delta opiate agonists on respiration. Eur. J. Pharmacol. 98(2), 235–240.

    PubMed  CAS  Google Scholar 

  70. Morin-Surun M.-P., Boudinot E., Dubois C., et al. (2001) Respiratory function in adult mice lacking the mu-opioid receptor: role of deltareceptors. Eur. J. Neurosci. 13(9), 1703–1710.

    PubMed  CAS  Google Scholar 

  71. Mellen N. M., Janczewski W. A., Bocchiaro C. M., and Feldman J. L. (2003) Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37(5), 821–826.

    PubMed  CAS  Google Scholar 

  72. Morin-Surun M. P., Boudinot E., Kato F., Foutz A. S., and Denavit-Saubié M. (1995) Involvement of NMDA receptors in the respiratory phase transition is different in the adult guinea pig in vivo and in the isolated brainstem preparation. J. Neurophysiol. 74, 770–778.

    PubMed  CAS  Google Scholar 

  73. Blanco C. E. (1994) Maturation of fetal breathing activity. Biol. Neonate 65, 182–188.

    PubMed  CAS  Google Scholar 

  74. Jansen A. H. and Chernick V. (1983) Development of respiratory control. Physiol. Rev. 63, 437–483.

    PubMed  CAS  Google Scholar 

  75. Ramirez J. M., Quellmalz U. J., and Richter D. W. (1996) Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice. J. Physiol. 491, 799–812.

    PubMed  CAS  Google Scholar 

  76. DeVries J. I. P., Visser G. H. A., and Prechtl H. F. R. (1982) The emergence of behavior. I. Qualitative aspects. Early Hum. Dev. 7, 301–322.

    CAS  Google Scholar 

  77. Suzue T. (1994) Mouse fetuses in late gestation maintained in vitro by transplacental. Neurosci. Res. 21, 173–176.

    PubMed  CAS  Google Scholar 

  78. Greer J. J., Smith J. C., and Feldman J.. (1992) Respiratory and locomotor patterns generated in the fetal rat brainstem-spinal cord in vitro. J. Neurophysiol. 67, 996–999.

    PubMed  CAS  Google Scholar 

  79. Fortin G., Champagnat J., and Lumsden A. (1994) Onset and maturation of branchiomotor activities in the chick hindbrain. NeuroReport 5(9), 1149–1152.

    PubMed  CAS  Google Scholar 

  80. Fortin G., Kato F., Lumsden A., and Champagnat J. (1995) Rhythm generation in the segmented hindbrain of chick embryos. J. Physiol. 486(3), 735–744.

    PubMed  CAS  Google Scholar 

  81. Clarke J. D. and Lumsden A. (1993) Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. Development 118, 151–162.

    PubMed  CAS  Google Scholar 

  82. Lumsden A., Clarke J. D. W., Keynes R., and Fraser S. (1994) Early phenotypic choices by neuronal precursors, revealed by clonal analysis of chick embryo hindbrain. Development 120(6), 1581–1589.

    PubMed  CAS  Google Scholar 

  83. Domínguez del Toro E., Borday V., Davenne M., Neun R., Rijli F. M., and Champagnat J. (2001) Generation of a novel functional neuronal circuit in Hoxa1 mutant mice. J. Neurosci. 21(15), 5637–5642.

    Google Scholar 

  84. Gavalas A., Trainor P., Ariza-McNaughton L., and Krumlauf R. (2001) Synergy between Hoxa1 and Hoxb1: the relationship between arch patterning and the generation of cranial neural crest. Development 128(15), 3017–3027.

    PubMed  CAS  Google Scholar 

  85. Popperl H., Bienz M., Studer M., Chan S. K., Aparicio S., Brenner S., Mann R. S., and Krumlauf R. (1995) Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81(7), 1031–1042.

    PubMed  CAS  Google Scholar 

  86. Di Rocco G., Mavilio F., and Zappavigna V. (1997) Functional dissection of a transcriptionally active, target-specific Hox-Pbx complex. EMBO J. 16(12), 3644–3654.

    PubMed  Google Scholar 

  87. Giudicelli F., Gilardi-Hebenstreit P., Mechta-Grigoriou F., Poquet C., and Charnay P. (2003) Novel activities of Mafb underlie its dual role in hindbrain segmentation and regional specification. Dev. Biol. 253, 150–162.

    PubMed  CAS  Google Scholar 

  88. Manzanares M., Trainor P. A., Nonchev S., et al. (1999) The role of kreisler in segmentation during hindbrain development. Dev. Biol. 211, 220–237.

    PubMed  CAS  Google Scholar 

  89. Voiculescu O., Taillebourg E., Pujades C., Kress C., Buart S., Charnay P., and Schneider-Maunoury S. (2001) Hindbrain patterning: Krox20 couples segmentation and specification of regional identity. Development 128, 4967–4978.

    PubMed  CAS  Google Scholar 

  90. Chatonnet F., Domínguez del Toro E., Voiculescu O., Charnay P., and Champagnat J. (2002) Different respiratory control systems are affected in homozygous and heterozygous kreisler mutant mice. Eur. J. Neurosci. 15, 684–692.

    PubMed  Google Scholar 

  91. Lund J. P., Kolta A., Westberg K. G., and Scott G. (1998) Brainstem mechanisms underlying feeding behaviors. Curr. Opin. Neurobiol. 8, 718–724.

    PubMed  CAS  Google Scholar 

  92. Jacquin T. D., Borday V., Schneider-Maunoury S., Topilko P., Ghilini G., Kato F., Charnay P., and Champagnat J. (1996) Reorganisation of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17, 747–758.

    PubMed  CAS  Google Scholar 

  93. Fortin G., Jungbluth S., Lumsden A., and Champagnat J. (1999) Segmental specification of GABAergic inhibition during development of hindbrain neural networks. Nat. Neurosci. 2, 873–877.

    PubMed  CAS  Google Scholar 

  94. Abadie V., Champagnat J., and Fortin F. (2000) Branchiomotor activities in mouse embryo. Neuroreport 11(1), 141–145.

    PubMed  CAS  Google Scholar 

  95. Dawes G. S., Gardner W. N., Johnston B. M., and Walker D. W. (1983) Breathing in fetal lambs: the effect of brainstem section. J. Physiol. 335, 535–553.

    PubMed  CAS  Google Scholar 

  96. Hanson M. A. (1988) The importance of baro- and chemoreflexes in the control of the fetal cardiovascular system. J. Dev. Physiol. 10(6), 491–511.

    PubMed  CAS  Google Scholar 

  97. Kinney H. C., Filiano J. J., Sleeper L. A., Mandell F., Valdes-Dapena M., and Frost White W. (1995) Decreased muscarinic receptor binding in the arcuate nucleus in sudden infant death syndrome. Science 269, 1446–1450.

    PubMed  CAS  Google Scholar 

  98. Vert P., Aranda J. V., Catz C., and Yaffe S. (1994) Control of breathing during development, Apnea of the newborn, and in Sudden Infant Death Syndrome: In Biol. Neonate (J. P. Relier, ed.). Karger, Basel, Switzerland, pp. 133–280.

    Google Scholar 

  99. Cortez S. C. and Kinney H. C. (1996) Brainstem tegmental necrosis and olivary hypoplasia: a lethal entity associated with congenital apnea. J. Neuropathol. Exp. Neurol. 55, 841–849.

    PubMed  CAS  Google Scholar 

  100. Erickson J. T., Conover J. C., Borday V., Champagnat J., and Katz D. M. (1996) Mice lacking BDNF exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J. Neurosci. 16, 5361–5371.

    PubMed  CAS  Google Scholar 

  101. Gozal D. and Harper R. M. (1999) Novel insights into congenital central hypoventilation syndrome. Curr. Opin. Pulm. Med. 5(6), 335–338.

    PubMed  CAS  Google Scholar 

  102. Abadie V., Champagnat J., Fortin G., and Couly G. (1999) Sucking-deglutition-respiration and brain stem development genes. Arch. Pediatr. 6, 1043–1047.

    PubMed  CAS  Google Scholar 

  103. Lijowska A., Reed N., Chiodini B., and Thach B. (1995) Sequential reflex behavior leading to airway defense maneuvers and arousal from sleep in infants. Respirat. Crit. Care Med. 151, A151.

    Google Scholar 

  104. Champagnat J. and Fortin G. (1996) Primordial respiratory-like rhythm generation in the vertebrate embryo. TINS 20, 119–124.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christelle Thaëron-Antôno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chatonnet, F., del Toro, E.D., Thoby-Brisson, M. et al. From hindbrain segmentation to breathing after birth. Mol Neurobiol 28, 277–293 (2003). https://doi.org/10.1385/MN:28:3:277

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/MN:28:3:277

Index Entries

Navigation