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Published in: Brain Structure and Function 8/2017

Open Access 01-11-2017 | Original Article

Nuclear derivatives and axonal projections originating from rhombomere 4 in the mouse hindbrain

Authors: Maria Di Bonito, Michèle Studer, Luis Puelles

Published in: Brain Structure and Function | Issue 8/2017

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Abstract

The r4-derived territory is located in the pontine region of the brainstem, forming a wedge-shaped slice that broadens from the choroidal roof to the ventral midline. R4-derived neuronal populations migrate radially inside and tangentially outside this rhombomere, forming nuclei of the sensorimotor auditory, vestibular, trigeminal and reticular systems. R4-derived fibre tracts contribute to the lateral lemniscus, the trigeminothalamic tracts, the medial tegmental tract and the medial forebrain bundle, which variously project to the midbrain, thalamus, hypothalamus and telencephalon. Other tracts such as the trigeminocerebellar and vestibulocerebellar tracts reach the cerebellum, while the medial and lateral vestibulospinal tracts, and the reticulospinal and trigeminal oro-spinal tracts extend into the spinal cord. Many r4-derived fibres are crossed; they decussate to the contralateral side traversing the midline through the cerebellar, collicular and intercollicular commissures, as well as the supraoptic decussation. Moreover, some fibres enter into the posterior and anterior commissures and some terminals reach the septum. Overall, this study provides an overview of all r4 neuronal populations and axonal tracts from their embryonic origin to the adult final location and target.
Literature
go back to reference Abrahams VC, Richmond FJ (1977) Motor role of the spinal projections of the trigeminal system. In: Anderson DJ, Matthews B (eds) Pain in the Trigeminal Region. Elsevier, Amsterdam, pp 405–411 Abrahams VC, Richmond FJ (1977) Motor role of the spinal projections of the trigeminal system. In: Anderson DJ, Matthews B (eds) Pain in the Trigeminal Region. Elsevier, Amsterdam, pp 405–411
go back to reference Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-Torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain Struct Funct 218:1229–1277 doi:10.1007/s00429-012-0456-8 CrossRefPubMed Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-Torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain Struct Funct 218:1229–1277 doi:10.​1007/​s00429-012-0456-8 CrossRefPubMed
go back to reference Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray, and the precerebellar reticular nuclei. J Comp Neurol 179:49–75. doi:10.1002/cne.901790105 CrossRefPubMed Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray, and the precerebellar reticular nuclei. J Comp Neurol 179:49–75. doi:10.​1002/​cne.​901790105 CrossRefPubMed
go back to reference Awatramani R, Soriano P, Rodriguez C, Mai JJ, Dymecki SM (2003) Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet 35:70–75. doi:10.1038/ng1228 CrossRefPubMed Awatramani R, Soriano P, Rodriguez C, Mai JJ, Dymecki SM (2003) Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet 35:70–75. doi:10.​1038/​ng1228 CrossRefPubMed
go back to reference Bassett JP, Taube JS (2005) Head direction signal generation: ascending and descending information streams. In: Wiener SI, Taube JS (eds) Head Direction Cells and the Neural Mechanisms of Spatial Orientation. MIT Press, Cambridge, pp 83–109 Bassett JP, Taube JS (2005) Head direction signal generation: ascending and descending information streams. In: Wiener SI, Taube JS (eds) Head Direction Cells and the Neural Mechanisms of Spatial Orientation. MIT Press, Cambridge, pp 83–109
go back to reference Blessing WW (1997) The lower brainstem and bodily homeostasis. Oxford Univ. Press, New York Blessing WW (1997) The lower brainstem and bodily homeostasis. Oxford Univ. Press, New York
go back to reference Bruce LL, Kingsley J, Nichols DH, Fritzsch B (1997) The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15:671–692CrossRefPubMed Bruce LL, Kingsley J, Nichols DH, Fritzsch B (1997) The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15:671–692CrossRefPubMed
go back to reference Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545CrossRefPubMed Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545CrossRefPubMed
go back to reference Dallel R, Raboisson P, Woda A, Sessle BJ (1990) Properties of nociceptive and non-nociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res 521:95–106CrossRefPubMed Dallel R, Raboisson P, Woda A, Sessle BJ (1990) Properties of nociceptive and non-nociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res 521:95–106CrossRefPubMed
go back to reference Dallel R, Duale C, Luccarini P, Molat JL (1999) Stimulus-function, wind-up and modulation by diffuse noxious inhibitory controls of responses of convergent neurons of the spinal trigeminal nucleus oralis. Eur J Neurosci 11:31–40CrossRefPubMed Dallel R, Duale C, Luccarini P, Molat JL (1999) Stimulus-function, wind-up and modulation by diffuse noxious inhibitory controls of responses of convergent neurons of the spinal trigeminal nucleus oralis. Eur J Neurosci 11:31–40CrossRefPubMed
go back to reference Devoize L, Domejean S, Melin C, Raboisson P, Artola A, Dallel R (2010) Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat: a neuroanatomical substrate for reciprocal orofacial-cervical interactions. Brain Res 1343:75–82. doi:10.1016/j.brainres.2010.04.076 CrossRefPubMed Devoize L, Domejean S, Melin C, Raboisson P, Artola A, Dallel R (2010) Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat: a neuroanatomical substrate for reciprocal orofacial-cervical interactions. Brain Res 1343:75–82. doi:10.​1016/​j.​brainres.​2010.​04.​076 CrossRefPubMed
go back to reference Di Meglio T, Kratochwil CF, Vilain N, Loche A, Vitobello A, Yonehara K, Hrycaj SM, Roska B, Peters AH, Eichmann A, Wellik D, Ducret S, Rijli FM (2013) Ezh2 orchestrates topographic migration and connectivity of mouse precerebellar neurons. Science 339:204–207. doi:10.1126/science.1229326 CrossRefPubMedPubMedCentral Di Meglio T, Kratochwil CF, Vilain N, Loche A, Vitobello A, Yonehara K, Hrycaj SM, Roska B, Peters AH, Eichmann A, Wellik D, Ducret S, Rijli FM (2013) Ezh2 orchestrates topographic migration and connectivity of mouse precerebellar neurons. Science 339:204–207. doi:10.​1126/​science.​1229326 CrossRefPubMedPubMedCentral
go back to reference Diaz C, Glover JC, Puelles L, Bjaalie JG (2003) The relationship between hodological and cytoarchitectonic organization in the vestibular complex of the 11-day chicken embryo. J Comp Neurol 457:87–105. doi:10.1002/cne.10528 CrossRefPubMed Diaz C, Glover JC, Puelles L, Bjaalie JG (2003) The relationship between hodological and cytoarchitectonic organization in the vestibular complex of the 11-day chicken embryo. J Comp Neurol 457:87–105. doi:10.​1002/​cne.​10528 CrossRefPubMed
go back to reference Fu Y, Tvrdik P, Makki N, Paxinos G, Watson C (2011) Precerebellar cell groups in the hindbrain of the mouse defined by retrograde tracing and correlated with cumulative Wnt1-cre genetic labeling. Cerebellum 10:570–584. doi:10.1007/s12311-011-0266-1 CrossRefPubMed Fu Y, Tvrdik P, Makki N, Paxinos G, Watson C (2011) Precerebellar cell groups in the hindbrain of the mouse defined by retrograde tracing and correlated with cumulative Wnt1-cre genetic labeling. Cerebellum 10:570–584. doi:10.​1007/​s12311-011-0266-1 CrossRefPubMed
go back to reference Fujiyama T, Yamada M, Terao M, Terashima T, Hioki H, Inoue YU, Inoue T, Masuyama N, Obata K, Yanagawa Y, Kawaguchi Y, Nabeshima Y, Hoshino M (2009) Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136:2049–2058 doi:10.1242/dev.033480 CrossRefPubMed Fujiyama T, Yamada M, Terao M, Terashima T, Hioki H, Inoue YU, Inoue T, Masuyama N, Obata K, Yanagawa Y, Kawaguchi Y, Nabeshima Y, Hoshino M (2009) Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136:2049–2058 doi:10.​1242/​dev.​033480 CrossRefPubMed
go back to reference Gaufo GO, Flodby P, Capecchi MR (2000) Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127:5343–5354PubMed Gaufo GO, Flodby P, Capecchi MR (2000) Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development 127:5343–5354PubMed
go back to reference Gavalas A, Ruhrberg C, Livet J, Henderson CE, Krumlauf R (2003) Neuronal defects in the hindbrain of Hoxa1, Hoxb1 and Hoxb2 mutants reflect regulatory interactions among these Hox genes. Development 130:5663–5679 doi:10.1242/dev.00802 CrossRefPubMed Gavalas A, Ruhrberg C, Livet J, Henderson CE, Krumlauf R (2003) Neuronal defects in the hindbrain of Hoxa1, Hoxb1 and Hoxb2 mutants reflect regulatory interactions among these Hox genes. Development 130:5663–5679 doi:10.​1242/​dev.​00802 CrossRefPubMed
go back to reference Hopkins DA (2005) Neuroanatomy of head direction cell circuits. In: S.I. W J.S. T (ed) Head Direction Cells and the Neural Mechanisms of Spatial Orientation. MIT Press, Cambridge, pp 83–109 Hopkins DA (2005) Neuroanatomy of head direction cell circuits. In: S.I. W J.S. T (ed) Head Direction Cells and the Neural Mechanisms of Spatial Orientation. MIT Press, Cambridge, pp 83–109
go back to reference Jones BE (1995) Reticular formation: cytoarchitecture, transmitters, and projections. In: Paxinos G (ed) The rat nervous system. 2nd edn. Academic Press, San Diego, pp 155–171 Jones BE (1995) Reticular formation: cytoarchitecture, transmitters, and projections. In: Paxinos G (ed) The rat nervous system. 2nd edn. Academic Press, San Diego, pp 155–171
go back to reference Jones BE, Yang TZ (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56–92. doi:10.1002/cne.902420105 CrossRefPubMed Jones BE, Yang TZ (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56–92. doi:10.​1002/​cne.​902420105 CrossRefPubMed
go back to reference Lorente de Nó R (1981) The primary acoustic nuclei. Raven Press, New York Lorente de Nó R (1981) The primary acoustic nuclei. Raven Press, New York
go back to reference Lorente-Canovas B, Marin F, Corral-San-Miguel R, Hidalgo-Sanchez M, Ferran JL, Puelles L, Aroca P (2012) Multiple origins, migratory paths and molecular profiles of cells populating the avian interpeduncular nucleus. Dev Biol 361:12–26. doi:10.1016/j.ydbio.2011.09.032 CrossRefPubMed Lorente-Canovas B, Marin F, Corral-San-Miguel R, Hidalgo-Sanchez M, Ferran JL, Puelles L, Aroca P (2012) Multiple origins, migratory paths and molecular profiles of cells populating the avian interpeduncular nucleus. Dev Biol 361:12–26. doi:10.​1016/​j.​ydbio.​2011.​09.​032 CrossRefPubMed
go back to reference Lumsden A (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 13:329–335CrossRefPubMed Lumsden A (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 13:329–335CrossRefPubMed
go back to reference Malmierca MS, Merchán MA (2004) Auditory system. In: Paxinos G (ed) The Rat Nervous System. 3rd edn. Academic Press, San Diego, pp 997–1082CrossRef Malmierca MS, Merchán MA (2004) Auditory system. In: Paxinos G (ed) The Rat Nervous System. 3rd edn. Academic Press, San Diego, pp 997–1082CrossRef
go back to reference Marin F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738CrossRefPubMed Marin F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738CrossRefPubMed
go back to reference Martinez-de-la-Torre M, Lambertos A, Peñafiel R, Puelles L (2017) An exercise in brain genoarchitectonics: analysis of Azin2-LacZ expressing neuronal populations in the mouse hindbrain. J Neurosci Res (in press) Martinez-de-la-Torre M, Lambertos A, Peñafiel R, Puelles L (2017) An exercise in brain genoarchitectonics: analysis of Azin2-LacZ expressing neuronal populations in the mouse hindbrain. J Neurosci Res (in press)
go back to reference Miguez A, Ducret S, Di Meglio T, Parras C, Hmidan H, Haton C, Sekizar S, Mannioui A, Vidal M, Kerever A, Nyabi O, Haigh J, Zalc B, Rijli FM, Thomas JL (2012) Opposing roles for Hoxa2 and Hoxb2 in hindbrain oligodendrocyte patterning. J Neurosci 32:17172–17185. doi:10.1523/JNEUROSCI.0885-12.2012 CrossRefPubMed Miguez A, Ducret S, Di Meglio T, Parras C, Hmidan H, Haton C, Sekizar S, Mannioui A, Vidal M, Kerever A, Nyabi O, Haigh J, Zalc B, Rijli FM, Thomas JL (2012) Opposing roles for Hoxa2 and Hoxb2 in hindbrain oligodendrocyte patterning. J Neurosci 32:17172–17185. doi:10.​1523/​JNEUROSCI.​0885-12.​2012 CrossRefPubMed
go back to reference Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E (2014) Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct 219:777–792 doi:10.1007/s00429-013-0534-6 CrossRefPubMed Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E (2014) Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct 219:777–792 doi:10.​1007/​s00429-013-0534-6 CrossRefPubMed
go back to reference Olsson KA, Sasamoto K, Lund JP (1986) Modulation of transmission in rostral trigeminal sensory nuclei during chewing. J Neurophysiol 55:56–75PubMed Olsson KA, Sasamoto K, Lund JP (1986) Modulation of transmission in rostral trigeminal sensory nuclei during chewing. J Neurophysiol 55:56–75PubMed
go back to reference Parrish M, Nolte C, Krumlauf H (2009) Hox gene expression. In: Lemke G (ed) Developmental neurobiology. Academic Press, New York, pp 61–71 Parrish M, Nolte C, Krumlauf H (2009) Hox gene expression. In: Lemke G (ed) Developmental neurobiology. Academic Press, New York, pp 61–71
go back to reference Pasqualetti M, Diaz C, Renaud JS, Rijli FM, Glover JC (2007) Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J Neurosci 27:9670–9681. doi:10.1523/JNEUROSCI.2189-07.2007 CrossRefPubMed Pasqualetti M, Diaz C, Renaud JS, Rijli FM, Glover JC (2007) Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J Neurosci 27:9670–9681. doi:10.​1523/​JNEUROSCI.​2189-07.​2007 CrossRefPubMed
go back to reference Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. 2nd edn. Academic press, San Diego Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. 2nd edn. Academic press, San Diego
go back to reference Puelles L (2013) Plan of the developing vertebrate nervous system relating embryology to the adult nervous system (prosomere model, overview of brain organization). In: Rubenstein JLR, Rakic P (eds) Comprehensive developmental neuroscience: patterning and cell type specification in the developing CNS and PNS. Academic Press, Amsterdam, pp 187–209CrossRef Puelles L (2013) Plan of the developing vertebrate nervous system relating embryology to the adult nervous system (prosomere model, overview of brain organization). In: Rubenstein JLR, Rakic P (eds) Comprehensive developmental neuroscience: patterning and cell type specification in the developing CNS and PNS. Academic Press, Amsterdam, pp 187–209CrossRef
go back to reference Puelles L, Rubenstein JL (2015) A new scenario of hypothalamic organization: rationale of new hypotheses introduced in the updated prosomeric model. In: Alvarez-Bolado G, Grinevich V, Puelles L (eds) Development of the Hypothalamus. Front. Neuroanat, Lausanne, pp 9–27. doi:10.3389/fnana.2015.00027. Puelles L, Rubenstein JL (2015) A new scenario of hypothalamic organization: rationale of new hypotheses introduced in the updated prosomeric model. In: Alvarez-Bolado G, Grinevich V, Puelles L (eds) Development of the Hypothalamus. Front. Neuroanat, Lausanne, pp 9–27. doi:10.​3389/​fnana.​2015.​00027.
go back to reference Puelles L, Martinez-de-la-Torre M, Bardet S, Rubenstein JLR (2012) Hypothalamus. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier Academic Press, San Diego, pp 221–312CrossRef Puelles L, Martinez-de-la-Torre M, Bardet S, Rubenstein JLR (2012) Hypothalamus. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier Academic Press, San Diego, pp 221–312CrossRef
go back to reference Raboisson P, Dallel R, Clavelou P, Sessle BJ, Woda A (1995) Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat. J Neurophysiol 73:496–505PubMed Raboisson P, Dallel R, Clavelou P, Sessle BJ, Woda A (1995) Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat. J Neurophysiol 73:496–505PubMed
go back to reference Ramon y Cajal S (1911) Texture du Systeme Nerveux de l’Homme et des Vertebrás. vol 2. Paris: Maloine, re-edit. 1954 Madrid: CSIC Ramon y Cajal S (1911) Texture du Systeme Nerveux de l’Homme et des Vertebrás. vol 2. Paris: Maloine, re-edit. 1954 Madrid: CSIC
go back to reference Simon H, Lumsden A (1993) Rhombomere-specific origin of the contralateral vestibulo-acoustic efferent neurons and their migration across the embryonic midline. Neuron 11:209–220CrossRefPubMed Simon H, Lumsden A (1993) Rhombomere-specific origin of the contralateral vestibulo-acoustic efferent neurons and their migration across the embryonic midline. Neuron 11:209–220CrossRefPubMed
go back to reference Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4CrossRefPubMedPubMedCentral Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4CrossRefPubMedPubMedCentral
go back to reference Storm R, Cholewa-Waclaw J, Reuter K, Bröhl D, Sieber M, Treier M, Müller T, Birchmeier C (2009) The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136:295–305 doi:10.1242/dev.027193 CrossRefPubMed Storm R, Cholewa-Waclaw J, Reuter K, Bröhl D, Sieber M, Treier M, Müller T, Birchmeier C (2009) The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136:295–305 doi:10.​1242/​dev.​027193 CrossRefPubMed
go back to reference Studer M, Popperl H, Marshall H, Kuroiwa A, Krumlauf R (1994) Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265:1728–1732CrossRefPubMed Studer M, Popperl H, Marshall H, Kuroiwa A, Krumlauf R (1994) Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265:1728–1732CrossRefPubMed
go back to reference Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384:630–634. doi:10.1038/384630a0 CrossRefPubMed Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384:630–634. doi:10.​1038/​384630a0 CrossRefPubMed
go back to reference Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R (1998) Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125:1025–1036PubMed Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R (1998) Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125:1025–1036PubMed
go back to reference Tan K, Le Douarin NM (1991) Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system. Anat Embryol (Berl) 183:321–343CrossRef Tan K, Le Douarin NM (1991) Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system. Anat Embryol (Berl) 183:321–343CrossRef
go back to reference Tomas-Roca L, Corral-San-Miguel R, Aroca P, Puelles L, Marin F (2016) Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features. Brain Struct Funct. doi:10.1007/s00429-014-0938-y PubMed Tomas-Roca L, Corral-San-Miguel R, Aroca P, Puelles L, Marin F (2016) Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features. Brain Struct Funct. doi:10.​1007/​s00429-014-0938-y PubMed
go back to reference Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. Ergebnisse der Anatomie und Entwicklungsgeschichte 41:3–87 Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. Ergebnisse der Anatomie und Entwicklungsgeschichte 41:3–87
go back to reference Veinante P, Jacquin MF, Deschenes M (2000) Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat. J Comp Neurol 420:233–243CrossRefPubMed Veinante P, Jacquin MF, Deschenes M (2000) Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat. J Comp Neurol 420:233–243CrossRefPubMed
go back to reference Vertes RP, Martin GF (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J Comp Neurol 275:511–541. doi:10.1002/cne.902750404 CrossRefPubMed Vertes RP, Martin GF (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J Comp Neurol 275:511–541. doi:10.​1002/​cne.​902750404 CrossRefPubMed
go back to reference Vertes RP, Martin GF, Waltzer R (1986) An autoradiographic analysis of ascending projections from the medullary reticular formation in the rat. Neuroscience 19:873–898CrossRefPubMed Vertes RP, Martin GF, Waltzer R (1986) An autoradiographic analysis of ascending projections from the medullary reticular formation in the rat. Neuroscience 19:873–898CrossRefPubMed
go back to reference Voiculescu O, Charnay P, Schneider-Maunoury S (2000) Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 26:123–126CrossRefPubMed Voiculescu O, Charnay P, Schneider-Maunoury S (2000) Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 26:123–126CrossRefPubMed
go back to reference Watson CR, Switzer RC 3rd (1978) Trigeminal projections to cerebellar tactile areas in the rat-origin mainly from n. interpolaris and n. principalis. Neurosci Lett 10:77–82CrossRefPubMed Watson CR, Switzer RC 3rd (1978) Trigeminal projections to cerebellar tactile areas in the rat-origin mainly from n. interpolaris and n. principalis. Neurosci Lett 10:77–82CrossRefPubMed
go back to reference Webb BD, Shaaban S, Gaspar H, Cunha LF, Schubert CR, Hao K, Robson CD, Chan WM, Andrews C, MacKinnon S, Oystreck DT, Hunter DG, Iacovelli AJ, Ye X, Camminady A, Engle EC, Jabs EW (2012) HOXB1 founder mutation in humans recapitulates the phenotype of Hoxb1-/- mice. Am J Hum Genet 91:171–179. doi:10.1016/j.ajhg.2012.05.018 CrossRefPubMedPubMedCentral Webb BD, Shaaban S, Gaspar H, Cunha LF, Schubert CR, Hao K, Robson CD, Chan WM, Andrews C, MacKinnon S, Oystreck DT, Hunter DG, Iacovelli AJ, Ye X, Camminady A, Engle EC, Jabs EW (2012) HOXB1 founder mutation in humans recapitulates the phenotype of Hoxb1-/- mice. Am J Hum Genet 91:171–179. doi:10.​1016/​j.​ajhg.​2012.​05.​018 CrossRefPubMedPubMedCentral
go back to reference Wingate RJ, Lumsden A (1996) Persistence of rhombomeric organisation in the postsegmental hindbrain. Development 122:2143–2152PubMed Wingate RJ, Lumsden A (1996) Persistence of rhombomeric organisation in the postsegmental hindbrain. Development 122:2143–2152PubMed
Metadata
Title
Nuclear derivatives and axonal projections originating from rhombomere 4 in the mouse hindbrain
Authors
Maria Di Bonito
Michèle Studer
Luis Puelles
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1416-0

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