Development of starburst cholinergic amacrine cells in the retina of Tupaia belangeri

“Starburst” cholinergic amacrines specify the response of direction‐selective ganglion cells to image motion. Here, development of cholinergic amacrines was studied in the tree shrew Tupaia belangeri (Scandentia) by immunohistochemistry with antibodies against choline acetyltransferase (ChAT) and neurofilament proteins. Starburst amacrines expressed ChAT much earlier than previously thought. From embryonic day 34 (E34) onward, orthotopic and displaced subpopulations segregated from a single cluster of immunoreactive precursor cells. Orthotopic starburst amacrines rapidly took up positions in the inner nuclear layer. Displaced starburst amacrines were first arranged in a monocellular row in the inner plexiform layer, and, with a delay of 1 week, they descended to the ganglion cell layer. Conversely, dendritic stratification of displaced amacrines slightly preceded that of orthotopic ones. Starburst amacrines expressed the medium‐molecular‐weight neurofilament protein (NF‐M) from E34 to postnatal day 11 (P11) and coexpressed α‐internexin from E36.5 to P11. Consequently, neurofilaments composed of α‐internexin and NF‐M may stabilize developing dendrites of starburst amacrines. During the first 2 postnatal weeks, subpopulations of anti‐NF‐M‐labeled ganglion cells costratified with the preexisting dendritic strata of starburst amacrines in the ON sublamina, OFF sublamina, or both. Hence, anti‐NF‐M‐labeled ganglion cells may include direction‐selective ones. Thereafter, NF‐M and α‐internexin proteins disappeared from starburst amacrines, and NF‐M immunoreactivity was lost in the dendrites of ganglion cells. Our findings suggest that NF‐M and α‐internexin are important for starburst amacrines and ganglion cells to recognize each other and, thus, contribute to the formation of early developing retinal circuits in the inner plexiform layer. J. Comp. Neurol. 502:584–597, 2007. © 2007 Wiley‐Liss, Inc.

[1]  M. Doldán,et al.  Immunochemical localization of calretinin in the retina of the turbot (Psetta maxima) during development , 1999, The Journal of comparative neurology.

[2]  G. Rager,et al.  Synaptogenesis in the primary visual cortex of the tree shrew (Tupaia belangeri) , 1991, The Journal of comparative neurology.

[3]  E. V. Famiglietti,et al.  Immunocytochemical staining of cholinergic amacrine cells in rabbit retina , 1987, Brain Research.

[4]  M. Ochs,et al.  To what extent are the retinal capillaries ensheathed by Müller cells? A stereological study in the tree shrew Tupaia belangeri , 2000, Journal of anatomy.

[5]  Sangmook Lee,et al.  The predominant form in which neurofilament subunits undergo axonal transport varies during axonal initiation, elongation, and maturation. , 2001, Cell motility and the cytoskeleton.

[6]  L. Chalupa,et al.  Segregation of On and Off Bipolar Cell Axonal Arbors in the Absence of Retinal Ganglion Cells , 2000, The Journal of Neuroscience.

[7]  L. Peichl,et al.  Unique Distribution of Somatostatin‐immunoreactive Cells in the Retina of the Tree Shrew (Tupaia belangeri) , 1996, The European journal of neuroscience.

[8]  D. Redburn-Johnson GABA as a developmental neurotransmitter in the outer plexiform layer of the vertebrate retina. , 1998, Perspectives on developmental neurobiology.

[9]  R. Liem,et al.  Roles of head and tail domains in alpha-internexin's self-assembly and coassembly with the neurofilament triplet proteins. , 1998, Journal of cell science.

[10]  Richard H. Masland,et al.  Starburst Cells Nondirectionally Facilitate the Responses of Direction-Selective Retinal Ganglion Cells , 2002, The Journal of Neuroscience.

[11]  L. Jen,et al.  Development of choline acetyltransferase-immunoreactive neurons in normal and intracranially transplanted retinas in rats. , 1991, Brain research. Developmental brain research.

[12]  H. M. Petry,et al.  Visual pigments of the tree shrew (Tupaia belangeri) and greater galago (Galago crassicaudatus): A microspectrophotometric investigation , 1990, Vision Research.

[13]  J. T. Erichsen,et al.  Immunocytochemical identification of photoreceptor populations in the tree shrew retina , 1993, Brain Research.

[14]  E. Fuchs,et al.  Social stress in tree shrews Effects on physiology, brain function, and behavior of subordinate individuals , 2002, Pharmacology Biochemistry and Behavior.

[15]  D. Tibboel,et al.  HIRSCHSPRUNG'S DISEASE STUDIED WITH MONOCLONAL ANTINEUROFILAMENT ANTIBODIES ON TISSUE SECTIONS , 1984, The Lancet.

[16]  E. Famiglietti Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells , 1987, Brain Research.

[17]  G. H. Jacobs,et al.  Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri) , 1986, Vision Research.

[18]  M. Wong-Riley,et al.  Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: Normal patterns and the effect of retinal impulse blockage , 1988, The Journal of comparative neurology.

[19]  J. Stone,et al.  Ontogeny of catecholaminergic and cholinergic cell distributions in the cat's retina , 1989, The Journal of comparative neurology.

[20]  E. Cheon,et al.  Choline acetyltransferase and acetylcholinesterase in the normal, developing and regenerating newt retinas. , 1999, Brain research. Developmental brain research.

[21]  Carl D. Johnson,et al.  Localization of choline acetyltransferase‐like immunoreactivity in the embryonic chick retina , 1987, The Journal of comparative neurology.

[22]  C. V. von Bartheld,et al.  Expression of nerve growth factor (NGF) receptors in the brain and retina of chick embryos: Comparison with cholinergic development , 1991, The Journal of comparative neurology.

[23]  J. Julien,et al.  Neurofilament Transport In Vivo Minimally Requires Hetero-Oligomer Formation , 2003, The Journal of Neuroscience.

[24]  G. Rager,et al.  Classes of axons and their distribution in the optic nerve of the tree shrew (Tupaia belangeri) , 1997, The Anatomical record.

[25]  S. Skatchkov,et al.  “Lens Mitochondria” in the Retinal Cones of the Tree-shrew Tupaia belangeri , 1997, Vision Research.

[26]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[27]  R. Veh,et al.  On the development of the stratification of the inner plexiform layer in the chick retina , 2003, The Journal of comparative neurology.

[28]  W. Gerlich,et al.  Pre-S1 Antigen-Dependent Infection of Tupaia Hepatocyte Cultures with Human Hepatitis B Virus , 2003, Journal of Virology.

[29]  W. Knabe,et al.  Ciliogenesis in photoreceptor cells of the tree shrew retina , 1997, Anatomy and Embryology.

[30]  W. Knabe,et al.  The role of microtubules and microtubule-organising centres during the migration of mitochondria. , 1996, Journal of anatomy.

[31]  M. A. Raven,et al.  Organization of the inner retina following early elimination of the retinal ganglion cell population: Effects on cell numbers and stratification patterns , 2001, Visual Neuroscience.

[32]  Frank S. Werblin,et al.  Mechanisms and circuitry underlying directional selectivity in the retina , 2002, Nature.

[33]  M. Ochs,et al.  Horizontal cells invest retinal capillaries in the tree shrew Tupaia belangeri , 1999, Cell and Tissue Research.

[34]  D. Park,et al.  Horizontal cells of the rat retina show choline acetyltransferase- and vesicular acetylcholine transporter-like immunoreactivities during early postnatal developmental stages , 1998, Neuroscience Letters.

[35]  E. Fuchs,et al.  Anterograde tracing of retinal afferents to the tree shrew hypothalamus and raphe , 2000, Brain Research.

[36]  H. Kuhn,et al.  Implantation, early placentation, and the chronology of embryogenesis in Tupaia belangeri , 1973, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[37]  Haidong D. Lu,et al.  Temporal modulation sensitivity of tree shrew retinal ganglion cells , 2003, Visual Neuroscience.

[38]  F. Werblin,et al.  Requirement for Cholinergic Synaptic Transmission in the Propagation of Spontaneous Retinal Waves , 1996, Science.

[39]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[40]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[41]  E. V. Famiglietti,et al.  Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction , 1991, The Journal of comparative neurology.

[42]  G. Jeyarasasingam,et al.  Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  R. Liem,et al.  The neuronal intermediate filament, alpha-internexin is transiently expressed in amacrine cells in the developing mouse retina. , 1995, Experimental eye research.

[44]  G. Rager,et al.  On the postnatal development of the striate cortex (V1) in the tree shrew (Tupaia belangeri) , 2006, The European journal of neuroscience.

[45]  Zhou Zj,et al.  Direct Participation of Starburst Amacrine Cells in Spontaneous Rhythmic Activities in the Developing Mammalian Retina , 1998 .

[46]  Richard H. Masland,et al.  The many roles of starburst amacrine cells , 2005, Trends in Neurosciences.

[47]  W. Knabe,et al.  Morphogenesis of megamitochondria in the retinal cone inner segments of Tupaia belangeri (Scandentia) , 1996, Cell and Tissue Research.

[48]  N. Moreno,et al.  Localization of choline acetyltransferase in the developing and adult retina of Xenopus laevis , 2002, Neuroscience Letters.

[49]  J. B. Hutchins,et al.  Development of the lateral geniculate nucleus: Interactions between retinal afferent, cytoarchitectonic, and glial cell process lamination in ferrets and tree shrews , 1990, The Journal of comparative neurology.

[50]  M. Conley,et al.  Terminations of individual optic tract fibers in the lateral geniculate nuclei of Galago crassicaudatus and Tupaia belangeri , 1987, The Journal of comparative neurology.

[51]  L. Peichl,et al.  Morphology and distribution of catecholaminergic amacrine cells in the cone‐dominated tree shrew retina , 1991, The Journal of comparative neurology.

[52]  M. Conley,et al.  Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): I. Nuclear subdivisions and retinal projections , 1993, The Journal of comparative neurology.

[53]  C. W. Oyster,et al.  The analysis of image motion by the rabbit retina , 1968, The Journal of physiology.

[54]  W. Knabe,et al.  Pattern of cell death during optic cup formation in the tree shrew Tupaia belangeri , 1998, The Journal of comparative neurology.

[55]  S. Mangel,et al.  Cation–chloride cotransporters mediate neural computation in the retina , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[56]  J. May,et al.  Immunohistochemical organization of the ventral lateral geniculate nucleus in the tree shrew , 1992, The Journal of comparative neurology.

[57]  G. Rager,et al.  Structure and postnatal development of photoreceptors and their synapses in the retina of the tree shrew (Tupaia belangen) , 1987, Cell and Tissue Research.

[58]  J. Stone,et al.  Catecholaminergic and cholinergic neurons in the developing retina of the rat , 1988, The Journal of comparative neurology.

[59]  B. Boycott,et al.  Alpha ganglion cells in mammalian retinae , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[60]  L. Peichl,et al.  Rod bipolar cells in the cone-dominated retina of the tree shrew Tupaia belangeri , 1991, Visual Neuroscience.

[61]  M. López-Gallardo,et al.  Spatiotemporal gradients of differentiation of chick retina types I and II cholinergic cells: Identification of a common postmitotic cell population , 1999, The Journal of comparative neurology.

[62]  G. Rager,et al.  Classes of neurons in relation to the laminar organization of the lateral geniculate nucleus in the tree shrew, Tupaia belangeri , 1987, The Journal of comparative neurology.

[63]  Wenzhi Sun,et al.  Dendritic relationship between starburst amacrine cells and direction‐selective ganglion cells in the rabbit retina , 2004, The Journal of physiology.

[64]  R. Wong,et al.  Developmental Changes in the Neurotransmitter Regulation of Correlated Spontaneous Retinal Activity , 2000, The Journal of Neuroscience.

[65]  A. Reichenbach,et al.  Müller glial cells of the tree shrew retina , 1995, The Journal of comparative neurology.

[66]  M. Conley,et al.  Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): II. Connections with the cortex, thalamus, and brainstem , 1993, The Journal of comparative neurology.

[67]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[68]  D. Redburn,et al.  Developmental neurotransmitters. Signals for shaping neuronal circuitry. , 1996, Investigative ophthalmology & visual science.

[69]  H. Blum,et al.  Efficient Infection of Primary Tupaia Hepatocytes with Purified Human and Woolly Monkey Hepatitis B Virus , 2001, Journal of Virology.

[70]  J. Kühne Rod receptors in the retina of Tupaia belangeri , 2004, Anatomy and Embryology.

[71]  D. Fitzpatrick,et al.  Laminar asymmetry in the distribution of choline acetyltransferase-immunoreactive neurons in the retina of the tree shrew (Tupaia belangeri) , 1986, Brain Research.

[72]  N. Grzywacz,et al.  Localization of choline acetyltransferase in the developing and adult turtle retinas , 2000, The Journal of comparative neurology.

[73]  D. Redburn Development of GABAergic neurons in the mammalian retina. , 1992, Progress in brain research.

[74]  J. Dann Cholinergic amacrine cells in the developing cat retina , 1989, The Journal of comparative neurology.

[75]  H. M. Petry,et al.  Psychophysical measurement of spectral sensitivity and color vision in red-light-reared tree shrews (Tupaia belangeri) , 1991, Vision Research.

[76]  B. Boycott,et al.  Alpha ganglion cells in the rabbit retina , 1987, The Journal of comparative neurology.

[77]  R. Anadón,et al.  Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula) , 2000, The Journal of comparative neurology.

[78]  R. Marc Neurochemical stratification in the inner plexiform layer of the vertebrate retina , 1986, Vision Research.

[79]  Eun-Jin Lee,et al.  Choline acetyltransferase‐immunoreactive neurons in the developing rat retina , 2000, The Journal of comparative neurology.

[80]  S. Wu,et al.  Development of cholinergic amacrine cells is visual activity‐dependent in the postnatal mouse retina , 2005, The Journal of comparative neurology.

[81]  Lenira Camargo de Moura Campos,et al.  Ontogeny of cholinergic amacrine cells in the opossum (Didelphis aurita) retina , 1999, International Journal of Developmental Neuroscience.

[82]  R. Liem,et al.  Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments , 1993, The Journal of cell biology.

[83]  J. M. Thijssen,et al.  Functional classification of cells in the optic tract of a tree shrew (Tupaia chinensis) , 1976, Experimental Brain Research.

[84]  E. Fuchs Social Stress in Tree Shrews as an Animal Model of Depression: An Example of a Behavioral Model of a CNS Disorder , 2005, CNS Spectrums.

[85]  M. Huentelman,et al.  Characterization of mitotic neurons derived from adult rat hypothalamus and brain stem. , 2002, Journal of neurophysiology.

[86]  C. Morgans,et al.  Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri , 1998, Visual Neuroscience.

[87]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[88]  D. Pow,et al.  The dendritic architecture of the cholinergic plexus in the rabbit retina: Selective labeling by glycine accumulation in the presence of sarcosine , 2000, The Journal of comparative neurology.

[89]  C. Shatz,et al.  Early functional neural networks in the developing retina , 1995, Nature.

[90]  W. Knabe,et al.  Disk formation in retinal cones of Tupaia belangeri (Scandentia) , 1998, Cell and Tissue Research.

[91]  L. Peichl,et al.  Starburst cholinergic amacrine cells in the tree shrew retina , 1997, The Journal of comparative neurology.

[92]  Z. J. Zhou,et al.  Direct Participation of Starburst Amacrine Cells in Spontaneous Rhythmic Activities in the Developing Mammalian Retina , 1998, The Journal of Neuroscience.

[93]  R. Stacy,et al.  Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina , 2003, The Journal of comparative neurology.

[94]  L. Puelles,et al.  Inverted (displaced) retinal amacrine cells and their embryonic development in the chick , 1977, Experimental Neurology.

[95]  E. Hogan,et al.  Ca2+ -mediated degradation of central nervous system (CNS) proteins: Topographic and species variation , 1987, Metabolic Brain Disease.

[96]  H. Wässle,et al.  Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[97]  L. Peichl,et al.  Topography of cones and rods in the tree shrew retina , 1989, The Journal of comparative neurology.

[98]  W. Knabe,et al.  Capillary-contacting horizontal cells in the retina of the tree shrew Tupaia belangeri belong to the mammalian type A , 2000, Cell and Tissue Research.

[99]  Veeranna,et al.  α-Internexin Is Structurally and Functionally Associated with the Neurofilament Triplet Proteins in the Mature CNS , 2006, The Journal of Neuroscience.

[100]  M. Sacher,et al.  Associations between intermediate filament proteins expressed in cultured dorsal root ganglion neurons , 1997, Journal of neuroscience research.