Abstract
In the last 10 years our concept of the developing diencephalon has changed dramatically. This is a consequence of an increasing number of morphological, chemoarchitectural, gene expression and experimental data that resist a satisfactory interpretation within the usual morphological schema suggested by textbooks, represented by the so-called columnar view of the vertebrate forebrain. The columnar paradigm was instaurated by Herrick (1910), who divided the vertebrate diencephalon into four superposed columns separated by ventricular sulci. This schema was later supported by numerous adherents, among which Kuhlenbeck played a singular role (Kuhlenbeck 1973, and earlier work reviewed therein). The four columns were called epithalamus, thalamus dorsalis, thalamus ventralis and hypothalamus (from dorsal to ventral). They were held to be longitudinal parts of the neural tube, though this view is only possible by arbitrary disregard of the notorius axial bending of the rostral neural tube at the cephalic flexure (Keyser 1972; Puelles and Rubenstein 1993; Puelles 1995). Among other problems (see Puelles 1995), this schema typically dealt poorly with the pretectum, causing many authors to fail to distinguish it adequately from the dorsal thalamus, the epithalamus or the midbrain roof. Various descriptive embryologists noticed over the years the difficulties of the columnar approach, favoring a segmental paradigm, but did not achieve a substantial impact with their alternative interpretations (Rendahl 1924; Tello 1934; Bergquist 1954; Coggeshall 1964; Keyser 1972; Gribnau and Geijsberts 1985). These, nevertheless, finally constituted the base of the present conceptions, together with parallel work on non-mammalian vertebrates.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Altman J, Bayer SA (1978) Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J Comp Neurol 182: 945–972
Altman J, Bayer SA (1979) Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. J Comp Neurol 188: 455–472
Angevine JB (1970) Time of neuron origin in the diencephalon of the mouse. An autoradio-graphic study. J Comp Neurol 139: 129–188
Avantaggiato V, Pandolfi PP, Ruthardt M, Hawe N, Acampora D, Pelicci PG, Simeone A (1995) Developmental analysis of murine Promyelocyte Leukemia Zinc Finger (PLZF) gene expression: implications for the neuromeric model of the forebrain organization. J Neurosci 15: 4927–4942
Bergquist H (1954) Ontogenesis of diencephalic nuclei in vertebrates. A comparative study. K Fysiogr Sallsk Lund Handl 6: 1–34
Bosse A, Zulch A, Becker MB, Torres M, Gomez-Skarmeta JL, Modolell J, Gruss P (1997) Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech Dev 69: 169–181
Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JLR (1993) Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13: 3155–3172
Bulfone A, Smiga SM, Shimamura K, Puelles L, Peterson A, Rubenstein JLR (1995) T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15: 63–78
Caballero-Bleda M, Fernandez B, Puelles L (1992) The pretectal complex of the rabbit: distribution of AChE and NADPH-diaphorase activities. Acta Anat 144: 7–16
Caballero-Bleda M, Lagares C, Fernandez B, Puelles L (1993) A chemoarchitectonically similar internal extension connects the rabbit intergeniculate leaflet to midline dorsal thalamic nuclei. J Hirnforsch 34: 33–40
Chazaud C, Oulad-Abdelghani M, Bouillet P, Decimo D, Chambon P, Dolle P (1996) AP-2.2, a novel gene related to AP-2, is expressed in the forebrain, limbs and face during mouse embryogenesis. Mech Dev 54: 83–94
Cho EA, Dressler GR (1998) TCF-4 binds beta-catenin and is expressed in distinct regions of the embryonic brain and limbs. Mech Dev 77: 9–18
Coggeshall RE (1964) A study of diencephalic development in the albino rat. J Comp Neurol 122: 241–269
Crossley PH, Martinez S, Martin GR (1996) Midbrain development induced by FGF8 in the chick embryo. Nature 380: 66–68
de Castro F, Cobos I, Puelles L, Martinez S (1998) Calretinin in pretecto- and olivocerebellar projections in the chick: immunohistochemical and experimental study. J Comp Neurol 397: 149–162
Fan C-M, Kuwana E, Bulfone A, Fletcher CF, Copeland NG, Jenkins NA, Crews S, Martinez S, Puelles L, Rubenstein JLR, Tessier-Lavigne M (1996) Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome. Mol Cell Neurosci 7: 1–16
Figdor MC, Stern CD (1993) Segmental organization of embryonic diencephalon. Nature 363: 630–634
Foster GA (1998) Chemical neuroanatomy of the prenatal rat brain. A developmental atlas. Oxford University Press, Oxford New York Tokyo
Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins ( BMPs) as regulators of dorsal forebrain development. Development 124: 2203–2212
Garel S, Marin F, Mattei MG, Vesque C, Vincent A, Charnay P (1997) Family of Ebf/Olf-l-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev Dyn 210: 191–205
Gribnau AAM, Geijsberts LGM (1985) Morphogenesis of the brain in staged Rhesus monkey embryos. Adv Anat Embryol Cell Biol 91: 1–69
Grindley JC, Hargett LK, Hill RE, Ross A, Hogan BL (1997) Disruption of PAX6 function in mice homozygous for the Pax6/Sey-1/Neu mutation produces abnormalities in the early development and regionalization of the diencephalon. Mech Dev 64: 111–126
Herrick CJ (1910) The morphology of the forebrain in amphibia and reptilia. J Comp Neurol 20: 413–545
His W (1893) Vorschläge zur Einteilung des Gehirns. Arch Anat Entwicklungsgesch 17: 172–179
Hsieh-Li HM, Witte DP, Szucsik JC, Weinstein M, Li H, Potter SS (1995) Gsh-2, a murine homeobox gene expressed in the developing brain. Mech Dev 50: 177–186
Jacobowitz DM, Abbott LC (1997) Chemoarchitectonic atlas of the developing mouse brain. CRC Press, Boca Raton
Keyser A (1972) The development of the diencephalon of the chinese hamster. Acta Anatomica 83: 1–181
Kitamura K, Miura H, Yanazawa M, Miyashita T, Kato K (1997) Expression patterns of Brxl (Rieg gene), Sonic hedgehog, Nkx2.2, Dlxl and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech Dev 67: 83–96
Korematsu K, Redies C (1997) Restricted expression of cadherin-8 in segmental and functional subdivisions of the embryonic mouse brain. Dev Dyn 208: 178–189
Kuhlenbeck H (1973) The central nervous system of vertebrates. Vol 3 Part I I. S Karger, Berlin
Lagares C, Caballero-Bleda M, Fernandez B, Puelles L (1994) Reciprocal connections between the rabbit suprageniculate pretectal nucleus and the superior colliculus: tracer study with horseradish peroxidase and Fluorogold. Visual Neurosci 11: 347–353
Lumsden A, Krumlauf R (1996) Patterning the vertebrate neuraxis. Science 274: 1109–1115
Martínez S, Wassef M, Alvarado-Mallart RM (1991) Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene Ent. Neuron 6: 971–981
Martínez S, Crossley PH, Cobos I, Rubenstein JLR, Martin GR (1999) FGF-8 induces an isthmic organizer and isthmocerebellar development in the caudal forebrain via a repressive effect on Otx2 expression. Development 126: 1189–1200
Mastick GS, Easter SE (1996) Initial organization of neurons and tracts in the embryonic mouse fore- and midbrain. Dev Biol 173: 79–94
Mellitzer G, Xu Q, Wilkinson DG (1999) Eph receptors and ephrins restricted cell intermingling and communication. Nature 400: 77–81
Miura H, Yanazawa M, Kato K, Kitamura K (1997) Expression of a novel aristaless related homeobox gene `Arx’ in the vertebrate telencephalon, diencephalon and floor plate. Mech Dev 65: 99–109
Miyashita-Lin EM, Hevner R, Wassarman KM, Martinez S, Martin GR, Rubenstein JLR (1999) Neocortical regionalization is preserved in the absence of thalamic innervation in newborn Gbx-2 mutant mice. Science 285: 906–909
Mucchielli ML, Martinez S, Pattyn A, Goridis C, Brunet JF (1996) Otlx-2, an Otx-related homeobox gene expressed in the pituitary gland and in a restricted pattern in the forebrain. Mol Cell Neurosci 8: 258–271
Nieuwenhuys R (1998) Morphogenesis and general structure. In: Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (eds) The Central Nervous System of Vertebrates, Vol I; chapter 4, pp 159–228. Springer, Berlin Heidelberg New York
Oliver G, Mailhos A, Wehr R, Copeland NG, Jenkins NA, Gruss P (1995) Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121: 4045–4055
Paxinos G, Ashwell KS, Törk Y (1994) Atlas of the developing rat nervous system. 2nd edn. Academic Press, London
Paxinos G, Kus L, Ashwell KS, Watson C (1999) Chemoarchitectonic Atlas of the Rat Brain. Academic Press, London
Platt KA, Michaud J, Joyner AL (1997) Expression of the mouse Gli and Ptc genes is adjacent to embryonic sources of hedgehog signals, suggesting a conservation of pathways between flies and mice. Mech Dev 62: 121–135
Pombal MA, Puelles L (1999) A prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, Nissl stain and ancillary markers. J Comp Neurol (in apress)
Price M, Lemaistre M, Pischetola M, Lauro RD, Duboule D (1991) A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351: 748–751
Puelles L (1995) A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav Evol 46: 319–337
Puelles L, Rubenstein JLR (1993) Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. TINS 16: 472–479
Puelles L, Amat JA, Martinez-de-la-Torre M (1987) Segment-related, mosaic neurogenetic pattern in the forebrain and mesencephalon of early chick embryos: I. Topography of AChEpositive neuroblasts up to stage HH18. J Comp Neurol 266: 247–268
Puelles L, Guillén M, Martinez de la Torre M (1991) Observations on the fate of nucleus superficialis magnocellularis of Rendahl in the avian diencephalon, bearing on the organization and nomenclature of neighboring retinorecipient nuclei. Anat Embryol 183: 221–233
Puelles L, Sanchez MP, Spreafico R, Fairen A (1992) Prenatal development of calbindin immunoreactivity in the dorsal thalamus of the rat. Neuroscience 46: 135–147
Redies C (1995) Cadherin expression in the developing vertebrate brain: from neuromeres to brain nuclei and neural circuits. Exp Brain Res 220: 243–256
Redies C, Takeichi M (1996) Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev Biol 180: 413–423
Rendahl H (1924) Embryologische and morphologische Studien über das Zwischenhirn beim Huhn. Acta Zool Stockh 5: 241–344
Robinson GW, Wray S, Mahon KA (1991) Spatially restricted expression of a member of a new family of murine distal-less homeobox genes in the developing forebrain. New Biologist 3: 1183–1194
Rubenstein JLR, Martinez S, Shimamura K, Puelles L (1994) The embryonic vertebrate forebrain: the prosomeric model. Science 266: 578–580
Rubenstein JLR, Shimamura K, Martinez S, Puelles L (1998) Regionalization of the prosencephalic neural plate. An Rev Neurosci 21: 445–477
Ruiz I, Altaba A (1998) Neural patterning. Deconstructing the organizer. Nature 391: 748–749
Salbaum JM (1998) Punc, a novel mouse gene of the immunoglobulin superfamily, is expressed predominantly in the developing nervous system. Mech Dev 71: 201–204
Sasaki H, Hogan BL (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118: 47–59
Schubert FR, Fainsod A, Gruenbaum Y, Gruss P (1995) Expression of the novel murine homeobox gene Sax-1 in the developing nervous system. Mech Dev 51: 99–114
Shimamura K, Rubenstein JLR (1997) Inductive interactions direct early regionalization of the mouse forebrain. Development 124: 2709–2718
Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JLR (1995) Longitudinal organization of the anterior neural plate and neural tube. Development 121: 3923–3933
Simeone A, Acampora D, Gulisano M, Stornaiuolo A, Boncinelli E (1992) Nested expression domains for homeobox genes in developing rostral brain. Nature 358: 687–690
Simeone A, Acampora D, Mallaci A, Stornaiuolo A, D’Apice MR, Nigro V, Boncinelli E (1993) A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 12: 2735–2747
Simeone A, D’Apice MR, Nigro V, Casanova J, Graziani G, Acampora D, Avantaggiato V (1994) Orthopedia, a novel gene homeobox-containing gene expressed in the developing central nervous system of both mouse and Drosophila. Neuron 13: 83
Stoykova A, Gruss P (1994) Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J Neurosci 14: 1395–1412
Stoykova A, Fritsch R, Walther C, Gruss P (1996) Forebrain patterning defects in small eye mutant mice. Development 122: 3453–3465
Swanson LW (1992) Brain Maps: Structure of the rat brain. Elsevier, Amsterdam
Tello JF (1934) Les differenciations neurofibrillaires dans le prosencephale de la souris de 4 a 15 millimetres. Tray Lab Rech Biol 29: 339–396
Timsit S, Martinez S, Allinquant B, Peyron F, Puelles L, Zalc B (1991) Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J Neurosci 15: 1012–1024
Uchikawa M, Kamachi Y, Kondo H (1999) Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 84: 103–120
Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). Ergeb Anat Entwicklungsgesch 41: 1–88
Zakin LD, Mazan S, Maury M, Martin N, Guenet JL, Brulet P (1998) Structure and expression of Wnt13, a novel mouse Wnt2 related gene. Mech Dev 73: 107–116
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Martínez, S., Puelles, L. (2000). Neurogenetic Compartments of the Mouse Diencephalon and some Characteristic Gene Expression Patterns. In: Goffinet, A.M., Rakic, P. (eds) Mouse Brain Development. Results and Problems in Cell Differentiation, vol 30. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-48002-0_4
Download citation
DOI: https://doi.org/10.1007/978-3-540-48002-0_4
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-53684-7
Online ISBN: 978-3-540-48002-0
eBook Packages: Springer Book Archive