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Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features

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Abstract

The medulla oblongata is the caudal portion of the vertebrate hindbrain. It contains major ascending and descending fiber tracts as well as several motor and interneuron populations, including neural centers that regulate the visceral functions and the maintenance of bodily homeostasis. In the avian embryo, it has been proposed that the primordium of this region is subdivided into five segments or crypto-rhombomeres (r7–r11), which were defined according to either their parameric position relative to intersomitic boundaries (Cambronero and Puelles, in J Comp Neurol 427:522–545, 2000) or a stepped expression of Hox genes (Marín et al., in Dev Biol 323:230–247, 2008). In the present work, we examine the implied similar segmental organization of the mouse medulla oblongata. To this end, we analyze the expression pattern of Hox genes from groups 3 to 8, comparing them to the expression of given cytoarchitectonic and molecular markers, from mid-gestational to perinatal stages. As a result of this approach, we conclude that the mouse medulla oblongata is segmentally organized, similarly as in avian embryos. Longitudinal structures such as the nucleus of the solitary tract, the dorsal vagal motor nucleus, the hypoglossal motor nucleus, the descending trigeminal and vestibular columns, or the reticular formation appear subdivided into discrete segmental units. Additionally, our analysis identified an internal molecular organization of the migrated pontine nuclei that reflects a differential segmental origin of their neurons as assessed by Hox gene expression.

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Abbreviations

5:

Trigeminal motor nucleus

6:

Abducens motor nucleus

6n:

Abducens nerve fibers

7:

Facial motor nucleus

7asc:

Ascending facial nerve fibers

7g:

Facial nerve genus

7n:

Descending facial nerve fibers

10:

Dorsal vagal motor nucleus

10n:

Vagal nerve fibers

12:

Hypoglossal motor nucleus

12n:

Hypoglossal nerve fibers

Amb:

Ambiguus motor nucleus

AP:

Area postrema

DC:

Dorsal cochlear nucleus

dcn:

Dorsal column nuclei

ECn:

External cuneate nucleus

Gi:

Gigantocellular reticular nucleus

IO:

Inferior olive

IRt:

Intermediate reticular nucleus

LRt:

Lateral reticular nucleus

MdV:

Ventral medullary reticular nucleus

MdD:

Dorsal medullary reticular nucleus

MVe:

Medial vestibular nucleus

mlf:

Medial longitudinal fascicle

PCRt:

Parvicellular reticular nucleus

pd:

Pyramidal decussation

Pn:

Basilar pontine nuclei

PnC:

Caudal pontine reticular nucleus

PnR:

Pontine raphe nucleus

Po:

Periolivary region

PPnR:

Prepontine raphe nucleus

Pr:

Prepositus nucleus

r:

Rhombomere

RAmb:

Retroambiguus nucleus

RMgV:

Raphe magnus nucleus, ventral part

RMgD:

Raphe magnus nucleus, dorsal part

Ro:

Roller nucleus

ROb:

Raphe obscurus nucleus

RPa:

Raphe pallidus nucleus

RtTg:

Reticular tegmental nucleus

RVL:

Rostroventrolateral reticular nucleus

sc:

Spinal cord

Sol:

Nucleus of the solitary tract

Sp5I:

Interpolar trigeminal nucleus

Sp5C:

Caudal trigeminal nucleus

SpVe:

Spinal vestibular nucleus

tz:

Trapezoid body

vh:

Ventral horn

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Acknowledgments

We thank C. Reyes Mendoza, M. Carmen Fernández, M. Carmen Morga and Isabel Piqueras for technical assistance. This study has been supported by a contract 04548-GERM-06 from the Fundación Séneca of the Government of the Murcia Region and grant MICINN-BFU2008-04156 from the Spanish Ministry of Science and Innovation to L.P. L.T-R. and R.C–S-M were recipient of respective predoctoral fellowships from the above-mentioned Fundación Séneca contract. We also thank RZPD, imaGenes GmbH and Geneservice Ltd for providing cDNA clones; and GenePaint.org, Allen Institute for Brain Science, and The Gene Expression Nervous System Atlas (GENSAT) database projects for providing part of the images analyzed in this work. The 3A10 antibody developed by T.M. Jessell and J. Dodd was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biology, Iowa City, IA, USA. cDNA clones were sequenced by the Molecular Biology Lab of the SAI (Servicio de Apoyo a la Investigación) at the University of Murcia.

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Authors and Affiliations

  1. Department of Human Anatomy and Psychobiology, School of Medicine, University of Murcia, and IMIB (Instituto Murciano de Investigación Biosanitaria), 30100, Murcia, Spain

    Laura Tomás-Roca, Rubén Corral-San-Miguel, Pilar Aroca, Luis Puelles & Faustino Marín

  2. Department of Human Genetics, Nijmegen Center for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands

    Laura Tomás-Roca

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  1. Laura Tomás-Roca
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Correspondence to Faustino Marín.

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Tomás-Roca, L., Corral-San-Miguel, R., Aroca, P. et al. Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features. Brain Struct Funct 221, 815–838 (2016). https://doi.org/10.1007/s00429-014-0938-y

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