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      The Long Adventurous Journey of Rhombic Lip Cells in Jawed Vertebrates: A Comparative Developmental Analysis

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          Abstract

          This review summarizes vertebrate rhombic lip and early cerebellar development covering classic approaches up to modern developmental genetics which identifies the relevant differential gene expression domains and their progeny. Most of this information is derived from amniotes. However, progress in anamniotes, particularly in the zebrafish, has recently been made. The current picture suggests that rhombic lip and cerebellar development in jawed vertebrates (gnathostomes) share many characteristics. Regarding cerebellar development, these include a ptf1a expressing ventral cerebellar proliferation (VCP) giving rise to Purkinje cells and other inhibitory cerebellar cell types, and an atoh1 expressing upper rhombic lip giving rise to an external granular layer (EGL, i.e., excitatory granule cells) and an early ventral migration into the anterior rhombencephalon (cholinergic nuclei). As for the lower rhombic lip (LRL), gnathostome commonalities likely include the formation of precerebellar nuclei (mossy fiber origins) and partially primary auditory nuclei (likely convergently evolved) from the atoh1 expressing dorsal zone. The fate of the ptf1a expressing ventral LRL zone which gives rise to (excitatory cells of) the inferior olive (climbing fiber origin) and (inhibitory cells of ) cochlear nuclei in amniotes, has not been determined in anamniotes. Special for the zebrafish in comparison to amniotes is the predominant origin of anamniote excitatory deep cerebellar nuclei homologs (i.e., eurydendroid cells) from ptf1a expressing VCP cells, the sequential activity of various atoh1 paralogs and the incomplete coverage of the subpial cerebellar plate with proliferative EGL cells. Nevertheless, the conclusion that a rhombic lip and its major derivatives evolved with gnathostome vertebrates only and are thus not an ancestral craniate character complex is supported by the absence of a cerebellum (and likely absence of its afferent and efferent nuclei) in jawless fishes

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          Cerebellar circuitry as a neuronal machine.

          Masao ITO (2006)
          Shortly after John Eccles completed his studies of synaptic inhibition in the spinal cord, for which he was awarded the 1963 Nobel Prize in physiology/medicine, he opened another chapter of neuroscience with his work on the cerebellum. From 1963 to 1967, Eccles and his colleagues in Canberra successfully dissected the complex neuronal circuitry in the cerebellar cortex. In the 1967 monograph, "The Cerebellum as a Neuronal Machine", he, in collaboration with Masao Ito and Janos Szentágothai, presented blue-print-like wiring diagrams of the cerebellar neuronal circuitry. These stimulated worldwide discussions and experimentation on the potential operational mechanisms of the circuitry and spurred theoreticians to develop relevant network models of the machinelike function of the cerebellum. In following decades, the neuronal machine concept of the cerebellum was strengthened by additional knowledge of the modular organization of its structure and memory mechanism, the latter in the form of synaptic plasticity, in particular, long-term depression. Moreover, several types of motor control were established as model systems representing learning mechanisms of the cerebellum. More recently, both the quantitative preciseness of cerebellar analyses and overall knowledge about the cerebellum have advanced considerably at the cellular and molecular levels of analysis. Cerebellar circuitry now includes Lugaro cells and unipolar brush cells as additional unique elements. Other new revelations include the operation of the complex glomerulus structure, intricate signal transduction for synaptic plasticity, silent synapses, irregularity of spike discharges, temporal fidelity of synaptic activation, rhythm generators, a Golgi cell clock circuit, and sensory or motor representation by mossy fibers and climbing fibers. Furthermore, it has become evident that the cerebellum has cognitive functions, and probably also emotion, as well as better-known motor and autonomic functions. Further cerebellar research is required for full understanding of the cerebellum as a broad learning machine for neural control of these functions.
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            Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum.

            Mikio Hoshino, Kazuwa Nakao, Akihisa Fukuda … (2005)
            The molecular machinery governing glutamatergic-GABAergic neuronal subtype specification is unclear. Here we describe a cerebellar mutant, cerebelless, which lacks the entire cerebellar cortex in adults. The primary defect of the mutant brains was a specific inhibition of GABAergic neuron production from the cerebellar ventricular zone (VZ), resulting in secondary and complete loss of external germinal layer, pontine, and olivary nuclei during development. We identified the responsible gene, Ptf1a, whose expression was lost in the cerebellar VZ but was maintained in the pancreas in cerebelless. Lineage tracing revealed that two types of neural precursors exist in the cerebellar VZ: Ptf1a-expressing and -nonexpressing precursors, which generate GABAergic and glutamatergic neurons, respectively. Introduction of Ptf1a into glutamatergic neuron precursors in the dorsal telencephalon generated GABAergic neurons with representative morphological and migratory features. Our results suggest that Ptf1a is involved in driving neural precursors to differentiate into GABAergic neurons in the cerebellum.
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              Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum.

              Lloyd F. Rose, Huda Zoghbi, Y Wang (2005)
              The rhombic lip (RL) is an embryonic proliferative neuroepithelium that generates several groups of hindbrain neurons. However, the precise boundaries and derivatives of the RL have never been genetically identified. We use beta-galactosidase expressed from the Math1 locus in Math1-heterozygous and Math1-null mice to track RL-derived cells and to evaluate their developmental requirements for Math1. We uncover a Math1-dependent rostral rhombic-lip migratory stream (RLS) that generates some neurons of the parabrachial, lateral lemniscal, and deep cerebellar nuclei, in addition to cerebellar granule neurons. A more caudal Math1-dependent cochlear extramural stream (CES) generates the ventral cochlear nucleus and cochlear granule neurons. Similarly, mossy-fiber precerebellar nuclei require Math1, whereas the inferior olive and locus coeruleus do not. We propose that Math1 expression delimits the extent of the rhombic lip and is required for the generation of the hindbrain superficial migratory streams, all of which contribute neurons to the proprioceptive/vestibular/auditory sensory network.
              Article 0 comments Cited 146 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Front Neuroanat
                Journal ID (publisher-id): Frontiers in Neuroanatomy
                Title: Frontiers in Neuroanatomy
                Publisher: Frontiers Research Foundation
                ISSN (Electronic): 1662-5129
                Publication date (Electronic preprint): 11 January 2011
                Publication date (Electronic): 21 April 2011
                Publication date Collection: 2011
                Volume: 5
                Electronic Location Identifier: 27
                Affiliations
                [1] 1simpleGraduate School of Systemic Neurosciences and Department Biology II, Ludwig–Maximilians-Universität Munich Planegg, Germany
                [2] 2simpleDepartment Developmental Biology, Institute of Biology I, University of Freiburg Freiburg, Germany
                [3] 3simpleInstitute of Developmental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health Neuherberg, Germany
                Author notes

                Edited by: Agustín González, Universidad Complutense de Madrid, Spain

                Reviewed by: Susan Dymecki, Harvard University, USA; Rob Machold, New York University School of Medicine, USA; Pilar Aroca, University of Murcia, Spain

                *Correspondence: Mario F. Wullimann, Graduate School of Systemic Neurosciences and Division of Neurobiology, Department Biology II, Ludwig–Maximilians-Universität Munich, Grosshadernerstr. 2, D-82152 Planegg, Bavaria, Germany. e-mail: wullimann@ 123456bio.lmu.de

                †Current address: Martin Distel, Department of Cellular and Molecular Medicine, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0380, USA; Reinhard W. Köster, Cell Biology and Cell Physiology, Institute of Zoology, Technische Universität Braunschweig, Spielmannstr. 7, D-38106 Braunschweig, Germany.

                Article
                DOI: 10.3389/fnana.2011.00027
                PMC ID: 3085262
                PubMed ID: 21559349
                SO-VID: 98c815b0-bc42-4b1a-ad23-70f8d5563552
                Copyright © Copyright © 2011 Wullimann, Mueller, Distel, Babaryka, Grothe and Köster.
                License:

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                Date received : 07 December 2010
                Date accepted : 06 April 2011
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 146, Pages: 16, Words: 14677
                Categories
                Subject: Neuroscience
                Subject: Review Article

                ScienceOpen disciplines: Neurosciences
                Keywords: wnt1,zebrafish,rhombic lip,ptf1a,cochlear nuclei,cerebellum,atoh1,precerebellar systems
                Data availability:
                ScienceOpen disciplines: Neurosciences
                Keywords: wnt1, zebrafish, rhombic lip, ptf1a, cochlear nuclei, cerebellum, atoh1, precerebellar systems

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