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<div class="pre-content"><div><div class="bk_prnt"><p class="small">NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.</p><p>Kolb H, Fernandez E, Jones B, et al., editors. Webvision: The Organization of the Retina and Visual System [Internet]. Salt Lake City (UT): University of Utah Health Sciences Center; 1995-. </p></div><div class="iconblock clearfix whole_rhythm no_top_margin bk_noprnt"><a class="img_link icnblk_img" title="Table of Contents Page" href="/books/n/webvision/"><img class="source-thumb" src="/corehtml/pmc/pmcgifs/bookshelf/thumbs/th-webvision-lrg.png" alt="Cover of Webvision" height="100px" width="80px" /></a><div class="icnblk_cntnt eight_col"><h2>Webvision: The Organization of the Retina and Visual System [Internet].</h2><a data-jig="ncbitoggler" href="#__NBK100303_dtls__">Show details</a><div style="display:none" class="ui-widget" id="__NBK100303_dtls__"><div>Kolb H, Fernandez E, Jones B, et al., editors.</div><div>Salt Lake City (UT): <a href="http://webvision.med.utah.edu/" ref="pagearea=page-banner&targetsite=external&targetcat=link&targettype=publisher">University of Utah Health Sciences Center</a>; 1995-.</div></div><div class="half_rhythm"><ul class="inline_list"><li style="margin-right:1em"><a class="bk_cntns" href="/books/n/webvision/">Contents</a></li></ul></div><div class="bk_noprnt"><form method="get" action="/books/n/webvision/" id="bk_srch"><div class="bk_search"><label for="bk_term" class="offscreen_noflow">Search term</label><input type="text" title="Search this book" id="bk_term" name="term" value="" data-jig="ncbiclearbutton" /> <input type="submit" class="jig-ncbibutton" value="Search this book" submit="false" style="padding: 0.1em 0.4em;" /></div></form></div></div><div class="icnblk_cntnt two_col"><div class="pagination bk_noprnt"><a class="active page_link prev" href="/books/n/webvision/ch21dev2/" title="Previous page in this title">< Prev</a><a class="active page_link next" href="/books/n/webvision/colorpercep/" title="Next page in this title">Next ></a></div></div></div></div></div>
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<div class="main-content lit-style" itemscope="itemscope" itemtype="http://schema.org/CreativeWork"><div class="meta-content fm-sec"><h1 id="_NBK100303_"><span class="title" itemprop="name">Development of Retinal Ganglion Cell Dendritic Structure and Synaptic Connections</span></h1><p class="contrib-group"><span itemprop="author">Ning Tian</span>, MD-PhD.</p><a data-jig="ncbitoggler" href="#__NBK100303_ai__" style="border:0;text-decoration:none">Author Information and Affiliations</a><div style="display:none" class="ui-widget" id="__NBK100303_ai__"><p class="contrib-group"><h4>Authors</h4><span itemprop="author">Ning Tian</span>, MD-PhD<sup><img src="/corehtml/pmc/pmcgifs/corrauth.gif" alt="corresponding author" /></sup><sup>1</sup>.</p><h4>Affiliations</h4><div class="affiliation"><sup>1</sup> Associate Professor of Ophthalmology and Neurobiology, Moran Eye Center, University of Utah School of Medicine.<div><span class="email-label">Email: </span><a href="mailto:dev@null" data-email="ude.hatu.csh@naiT.gniN" class="oemail">ude.hatu.csh@naiT.gniN</a></div></div><div><sup><img src="/corehtml/pmc/pmcgifs/corrauth.gif" alt="corresponding author" /></sup>Corresponding author.</div></div><p class="small">Created: <span itemprop="datePublished">June 13, 2012</span>.</p></div><div class="jig-ncbiinpagenav body-content whole_rhythm" data-jigconfig="allHeadingLevels: ['h2'],smoothScroll: false" itemprop="text"><div id="NingRGCD.1_Introduction"><h2 id="_NingRGCD_1_Introduction_">1. Introduction</h2><p>The neuronal information of the visual scene that is processed by the retina is conducted to the brain by a set of separate spatio-temporal synaptic pathways. The morphological basis for the formation of these parallel synaptic pathways is the laminar-specific structure of the retina, in which specific subtypes of retinal neurons form synapses only with highly selective presynaptic and postsynaptic cells (<a class="bk_pop" href="#NingRGCD.REF.1" data-bk-pop-others="NingRGCD.REF.2 NingRGCD.REF.3">1-3</a>).</p><p>Retinal ganglion cells (RGCs) are the output neurons of the retina. In the retina, RGCs synapse with bipolar and amacrine cells in the inner plexiform layer (IPL) to receive excitatory and inhibitory synaptic inputs respectively. The axons of RGCs travel through the optic nerve to retinorecipient structures in the brain, where they transfer their specific aspects of visual information to the higher centers (<a class="bk_pop" href="#NingRGCD.REF.3">3</a>). Because different subtypes of bipolar cells (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F1/?report=objectonly" target="object" rid-figpopup="figNingRGCDF1" rid-ob="figobNingRGCDF1">Fig 1</a>) (<a class="bk_pop" href="#NingRGCD.REF.4">4</a>) and amacrine cells (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F2/?report=objectonly" target="object" rid-figpopup="figNingRGCDF2" rid-ob="figobNingRGCDF2">Fig. 2</a>) (<a class="bk_pop" href="#NingRGCD.REF.5">5</a>) have their axonal/dendritic terminals in the specific sublaminae of the IPL, it is crucial that dendrites of individual RGCs are also confined to specific strata in order to synapses with them.</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF1" co-legend-rid="figlgndNingRGCDF1"><a href="/books/NBK100303/figure/NingRGCD.F1/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF1" rid-ob="figobNingRGCDF1"><img class="small-thumb" src="/books/NBK100303/bin/figure1.gif" src-large="/books/NBK100303/bin/figure1.jpg" alt="Figure 1: The major subtypes of bipolar cells of primate retina (Adapted from Wässle, 2004 (10))" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF1"><h4 id="NingRGCD.F1"><a href="/books/NBK100303/figure/NingRGCD.F1/?report=objectonly" target="object" rid-ob="figobNingRGCDF1">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 1: The major subtypes of bipolar cells of primate retina (Adapted from Wässle, 2004 (10)). Similar types have been observed in the rats (4), rabbit, cat (15, 74), monkey (75) and human (76). </p></div></div><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF2" co-legend-rid="figlgndNingRGCDF2"><a href="/books/NBK100303/figure/NingRGCD.F2/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF2" rid-ob="figobNingRGCDF2"><img class="small-thumb" src="/books/NBK100303/bin/figure2.gif" src-large="/books/NBK100303/bin/figure2.jpg" alt="Figure 2" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF2"><h4 id="NingRGCD.F2"><a href="/books/NBK100303/figure/NingRGCD.F2/?report=objectonly" target="object" rid-ob="figobNingRGCDF2">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 2. Schematic drawings of some of the amacrine cells of rabbit retina show each type has a characteristic morphology and stratification of the dendrites to specific strata (1-5) of the inner plexiform layer. All other mammals have similar cells. <a href="/books/NBK100303/figure/NingRGCD.F2/?report=objectonly" target="object" rid-ob="figobNingRGCDF2">(more...)</a></p></div></div><p>Thus, the synaptic circuitries processing distinct visual features, the so called “parallel pathways” (<a class="bk_pop" href="#NingRGCD.REF.1" data-bk-pop-others="NingRGCD.REF.2 NingRGCD.REF.6 NingRGCD.REF.7 NingRGCD.REF.8 NingRGCD.REF.9 NingRGCD.REF.10">1, 2, 6-10</a>), start in the retina. In most mammals, RGCs can be divided into about 20 morphological subtypes based on their distinctive dendritic structure and synaptic connections (<a class="bk_pop" href="#NingRGCD.REF.11" data-bk-pop-others="NingRGCD.REF.12 NingRGCD.REF.13 NingRGCD.REF.14 NingRGCD.REF.15 NingRGCD.REF.16 NingRGCD.REF.17 NingRGCD.REF.18 NingRGCD.REF.19">11-19</a>). The wholemount drawings of mouse RGCs (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F3/?report=objectonly" target="object" rid-figpopup="figNingRGCDF3" rid-ob="figobNingRGCDF3">Fig. 3</a>) illustrate the diversity of morphologies present in mammalian RGCs ((19). See also RGCs of human, cat and rabbit retinas in <a href="/books/n/webvision/ch07gc1/">the ganglion cell chapter in Webvision</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF3" co-legend-rid="figlgndNingRGCDF3"><a href="/books/NBK100303/figure/NingRGCD.F3/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF3" rid-ob="figobNingRGCDF3"><img class="small-thumb" src="/books/NBK100303/bin/Figure3.gif" src-large="/books/NBK100303/bin/Figure3.jpg" alt="Figure 3" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF3"><h4 id="NingRGCD.F3"><a href="/books/NBK100303/figure/NingRGCD.F3/?report=objectonly" target="object" rid-ob="figobNingRGCDF3">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 3. About 22 subtypes of retinal ganglion cells (RGCs) are present in the mammalian retina (See chapter on ganglion cells, Webvision). Camera lucida drawings show the RGCs of mouse retina. Adapted from Volgyi et al., 2009 (19). </p></div></div><p>Most of these RGCs have specific dendritic distribution in the IPL in adult retina as exemplified by the schematic (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F4/?report=objectonly" target="object" rid-figpopup="figNingRGCDF4" rid-ob="figobNingRGCDF4">Fig. 4</a>) showing the branching patterns of mouse RGCs. In most mammals, these lamina-restricted distributions of RGC dendrites and synaptic connections are formed during pre- and post-natal development. The question is how this lamination arises.</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF4" co-legend-rid="figlgndNingRGCDF4"><a href="/books/NBK100303/figure/NingRGCD.F4/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF4" rid-ob="figobNingRGCDF4"><img class="small-thumb" src="/books/NBK100303/bin/figure4.gif" src-large="/books/NBK100303/bin/figure4.jpg" alt="Figure 4" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF4"><h4 id="NingRGCD.F4"><a href="/books/NBK100303/figure/NingRGCD.F4/?report=objectonly" target="object" rid-ob="figobNingRGCDF4">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 4. Dendritic ramification depth of the 22 mouse RGC subtypes (From Volgi et al., 2009 (19)). Solid horizontal lines represent the inner and outer borders of the IPL, whereas dashed lines separate the 5 IPL strata. Numbers on the left represent <a href="/books/NBK100303/figure/NingRGCD.F4/?report=objectonly" target="object" rid-ob="figobNingRGCDF4">(more...)</a></p></div></div></div><div id="NingRGCD.2_Neurogenesis_and_synaptogenes"><h2 id="_NingRGCD_2_Neurogenesis_and_synaptogenes_">2. Neurogenesis and synaptogenesis of retina</h2><p>The neurogenesis and synaptogenesis of mammalian retina is an orderly process. <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-figpopup="figNingRGCDF5" rid-ob="figobNingRGCDF5">Figure 5</a> shows an overview drawing of the development of mouse retinal neurons. RGCs differentiate first followed by amacrine cells, cones and horizontal cells. Rod photoreceptors differentiate shortly afterward. Bipolar cells are the last neurons to differentiate. In mammals most retinal neurons differentiate before birth (<a class="bk_pop" href="#NingRGCD.REF.20" data-bk-pop-others="NingRGCD.REF.21 NingRGCD.REF.22">20-22</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF5" co-legend-rid="figlgndNingRGCDF5"><a href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF5" rid-ob="figobNingRGCDF5"><img class="small-thumb" src="/books/NBK100303/bin/Figure5.gif" src-large="/books/NBK100303/bin/Figure5.jpg" alt="Figure 5" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF5"><h4 id="NingRGCD.F5"><a href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-ob="figobNingRGCDF5">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 5. In mouse retina, neurogenesis begins before birth and is largely completed shortly after birth (A.). However neurogenesis of rods and bipolar cells starts before birth and continues for 1-2 weeks after birth (77). B: Synaptogenesis of mouse <a href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-ob="figobNingRGCDF5">(more...)</a></p></div></div><p>The order of synaptogenesis of retinal neurons is somewhat different from the order of neurogenesis. The synapses of amacrine cells in the IPL appear first. These are followed by the synaptic formation between photoreceptors and horizontal cells in the OPL. The last synaptic element to link photoreceptors in the outer retina and RGCs in the inner retina is the synaptic connection between bipolar cells and RGCs (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-figpopup="figNingRGCDF5" rid-ob="figobNingRGCDF5">Fig. 5A</a>) (<a class="bk_pop" href="#NingRGCD.REF.23" data-bk-pop-others="NingRGCD.REF.24">23, 24</a>). In mouse, the density of both ribbons and conventional synapses in the IPL continuously increases after eye opening and reaches the peak level by the age of P21 (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-figpopup="figNingRGCDF5" rid-ob="figobNingRGCDF5">Fig. 5B</a>). Functionally, the strength of RGC synaptic inputs measured by the frequency of spontaneous synaptic activity is low before eye opening in mice. After eye opening, a surge of glutamate receptor-mediated spontaneous excitatory postsynaptic currents (sEPSCs) and GABA/glycine receptor-mediated spontaneous inhibitory postsynaptic currents emerges around P25 (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F5/?report=objectonly" target="object" rid-figpopup="figNingRGCDF5" rid-ob="figobNingRGCDF5">Fig. 5B</a>). Amplitudes of RGC light responses in cat and ferret retina are also found to increase after eye opening (<a class="bk_pop" href="#NingRGCD.REF.25" data-bk-pop-others="NingRGCD.REF.26">25, 26</a>). In rabbit and rat, the amplitudes of retinal light responses measured by electroretinography continuously increases in the first month after birth and reaches the adult level by the ages of P30 to P40 (<a class="bk_pop" href="#NingRGCD.REF.27" data-bk-pop-others="NingRGCD.REF.28">27, 28</a>).</p><p>During synaptogenesis, the dendrites of mouse RGCs undergo very active remodeling. More than 30% of dendritic filopodial branches in the mouse are replaced every hour by continuous dendritic growth and elimination (pruning) between P10-13 (see <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F6/?report=objectonly" target="object" rid-figpopup="figNingRGCDF6" rid-ob="figobNingRGCDF6">Fig 6</a> and <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.Movie1/?report=objectonly" target="object" rid-figpopup="figNingRGCDMovie1" rid-ob="figobNingRGCDMovie1">movie 1</a>). This developmental remodeling of RGC dendrites is thought to play an important role in synaptogenesis and the formation of lamina-restricted dendritic distributions of RGCs.</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF6" co-legend-rid="figlgndNingRGCDF6"><a href="/books/NBK100303/figure/NingRGCD.F6/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF6" rid-ob="figobNingRGCDF6"><img class="small-thumb" src="/books/NBK100303/bin/Figure6.gif" src-large="/books/NBK100303/bin/Figure6.jpg" alt="Figure 6: Dendrites of mouse RGCs undergo very active remodeling during synaptogenesis in postnatal development" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF6"><h4 id="NingRGCD.F6"><a href="/books/NBK100303/figure/NingRGCD.F6/?report=objectonly" target="object" rid-ob="figobNingRGCDF6">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 6: Dendrites of mouse RGCs undergo very active remodeling during synaptogenesis in postnatal development. RGC dendritic motility was examined using time-lapse confocal imaging on retinas of YFP+ mice at P13-14. A: Representative image of an A1 <a href="/books/NBK100303/figure/NingRGCD.F6/?report=objectonly" target="object" rid-ob="figobNingRGCDF6">(more...)</a></p></div></div><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDMovie1" co-legend-rid="figlgndNingRGCDMovie1"><a href="/books/NBK100303/figure/NingRGCD.Movie1/?report=objectonly" target="object" title="Movie 1" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDMovie1" rid-ob="figobNingRGCDMovie1"><img class="small-thumb" src="/books/NBK100303/bin/FilapodiaMovieFrame1.gif" src-large="/books/NBK100303/bin/FilapodiaMovieFrame1.jpg" alt="Movie 1. Changes in filopodial growth and shape in the course of one hour." /></a><div class="icnblk_cntnt" id="figlgndNingRGCDMovie1"><h4 id="NingRGCD.Movie1"><a href="/books/NBK100303/figure/NingRGCD.Movie1/?report=objectonly" target="object" rid-ob="figobNingRGCDMovie1">Movie 1</a></h4><p class="float-caption no_bottom_margin">Changes in filopodial
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growth and shape in the course of one hour. </p></div></div></div><div id="NingRGCD.3_Formation_of_laminarestricted"><h2 id="_NingRGCD_3_Formation_of_laminarestricted_">3. Formation of lamina-restricted dendritic distributions of RGCs</h2><p>Many studies have shown that the dendritic morphology and synaptic connections of RGCs undergo profound refinement during postnatal development. Early in postnatal development, the dendrites of many RGCs ramify diffusely throughout the IPL of the retina in cats, rats and mice (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F7/?report=objectonly" target="object" rid-figpopup="figNingRGCDF7" rid-ob="figobNingRGCDF7">Fig. 7, A1, A2</a>). With subsequent maturation, RGC dendrites become much more narrowly stratified in the IPL (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F7/?report=objectonly" target="object" rid-figpopup="figNingRGCDF7" rid-ob="figobNingRGCDF7">Fig. 7, A2, B2 and B3</a>) (<a class="bk_pop" href="#NingRGCD.REF.26" data-bk-pop-others="NingRGCD.REF.29 NingRGCD.REF.30 NingRGCD.REF.31 NingRGCD.REF.32 NingRGCD.REF.33 NingRGCD.REF.34">26, 29-34</a>) at least partially due to a developmental restriction of RGC dendrites (<a class="bk_pop" href="#NingRGCD.REF.31">31</a>). Recent studies suggest that different subtypes of RGCs acquire their lamina-restricted dendritic ramification patterns in different ways.</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF7" co-legend-rid="figlgndNingRGCDF7"><a href="/books/NBK100303/figure/NingRGCD.F7/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF7" rid-ob="figobNingRGCDF7"><img class="small-thumb" src="/books/NBK100303/bin/Figure7.gif" src-large="/books/NBK100303/bin/Figure7.jpg" alt="Figure 7: Dendrites of RGCs can reach mature stratified pattern through selective pruning" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF7"><h4 id="NingRGCD.F7"><a href="/books/NBK100303/figure/NingRGCD.F7/?report=objectonly" target="object" rid-ob="figobNingRGCDF7">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 7: Dendrites of RGCs can reach mature stratified pattern through selective pruning. A1 and A2: Light micrographs of DiI (1,10-dioctadecyl-3,3,30,30-tetramethyl indocarbocyanine perchlorate) labeled RGCs from transverse sections of the central region <a href="/books/NBK100303/figure/NingRGCD.F7/?report=objectonly" target="object" rid-ob="figobNingRGCDF7">(more...)</a></p></div></div><p>Some RGCs seem to achieve their restricted lamina patterns by direct targeting without significant pruning. In <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F8/?report=objectonly" target="object" rid-figpopup="figNingRGCDF8" rid-ob="figobNingRGCDF8">Figure 8 A1-A3</a>, a bistratified RGC has a bistratified dendritic distribution pattern early at P5 (A1) and retains this bistratified pattern into adulthood (A2 and A3) without an initial diffuse distribution pattern. Similarly in Zebrafish some RGCs directly elaborate their dendrites to the middle of the IPL and later became strictly monostratified, occupying a single stratum in the middle of the IPL (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F8/?report=objectonly" target="object" rid-figpopup="figNingRGCDF8" rid-ob="figobNingRGCDF8">Fig. 8 B1, B2 and B3</a>) (<a class="bk_pop" href="#NingRGCD.REF.35">35</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF8" co-legend-rid="figlgndNingRGCDF8"><a href="/books/NBK100303/figure/NingRGCD.F8/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF8" rid-ob="figobNingRGCDF8"><img class="small-thumb" src="/books/NBK100303/bin/Figure8.gif" src-large="/books/NBK100303/bin/Figure8.jpg" alt="Figure 8" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF8"><h4 id="NingRGCD.F8"><a href="/books/NBK100303/figure/NingRGCD.F8/?report=objectonly" target="object" rid-ob="figobNingRGCDF8">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 8. Dendrites of RGCs can reach mature stratified pattern by direct targeting. A1, A2 and A3: Retinal sections from P5, P8, and P12-P13 BD mice, respectively. RGCs were labeled with anti-GFP (green) and starburst amacrines with anti-ChAT (red). <a href="/books/NBK100303/figure/NingRGCD.F8/?report=objectonly" target="object" rid-ob="figobNingRGCDF8">(more...)</a></p></div></div><p>It is also clear that some RGCs form their lamina-restricted dendritic patterns through both direct targeting and selective dendritic pruning (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" rid-figpopup="figNingRGCDF9" rid-ob="figobNingRGCDF9">Fig. 9</a>). In <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" rid-figpopup="figNingRGCDF9" rid-ob="figobNingRGCDF9">Figure 9, A1-A3</a>, the dendritic trees of a subtype of RGCs are diffusely ramified with many side branches originally and become bistratified to two strata above and below the cholinergic starburst type a cell with significant pruning of their dendritic branches (<a class="bk_pop" href="#NingRGCD.REF.33">33</a>). Similarly in <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" rid-figpopup="figNingRGCDF9" rid-ob="figobNingRGCDF9">Figure 9 B1-B3</a>, a zebrafish RGC starts its dendrites in the inner strata of the IPL and then selectively prunes the dendrites in the inner strata and grows the dendrites in the outer strata of the IPL over time (<a class="bk_pop" href="#NingRGCD.REF.35">35</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF9" co-legend-rid="figlgndNingRGCDF9"><a href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF9" rid-ob="figobNingRGCDF9"><img class="small-thumb" src="/books/NBK100303/bin/Figure9.gif" src-large="/books/NBK100303/bin/Figure9.jpg" alt="Figure 9" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF9"><h4 id="NingRGCD.F9"><a href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" rid-ob="figobNingRGCDF9">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 9. Dendrites of RGCs can reach mature stratified pattern by targeted growth and selective pruning. A1, A2 and A3: Retinal sections from P5, P8, and P12-P13 W7 mice, respectively. RGCs were labeled with anti-GFP (green) and starburst amacrines with <a href="/books/NBK100303/figure/NingRGCD.F9/?report=objectonly" target="object" rid-ob="figobNingRGCDF9">(more...)</a></p></div></div></div><div id="NingRGCD.4_Regulation_of_the_formation_o"><h2 id="_NingRGCD_4_Regulation_of_the_formation_o_">4. Regulation of the formation of lamina-restricted dendritic patterns of RGCs</h2><p>The regulatory mechanisms for the formation of the lamina-restricted dendritic patterns of RGCs are not completely understood. It has been reported that many molecular cues play crucial roles in the formation of laminar-restricted dendritic pattern of some subtypes of RGCs. The immunoglobulin superfamily adhesion molecules, DSCAMs and sidekicks, have been reported to direct laminar-specific axonal and dendritic ramification of bipolar cells and RGCs in chick retina (<a class="bk_pop" href="#NingRGCD.REF.36">36</a>) and RGC neurite arborization and mosaic formation in mouse retina (<a class="bk_pop" href="#NingRGCD.REF.37">37</a>). The transmembrane semaphorin Sema6A and its receptor PlexinA4 (PlexA4) have also been reported to control the stratification of the dendrites of dopaminergic amacrine cells, melanopsin containing RGCs and calbindin-positive cells into ON and OFF sublaminae of the IPL in mouse retina (<a class="bk_pop" href="#NingRGCD.REF.38">38</a>). <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F10/?report=objectonly" target="object" rid-figpopup="figNingRGCDF10" rid-ob="figobNingRGCDF10">Fig 10A</a> shows that transmembrane semaphorin Sema5A and Sema5B normally constrain dendritic targeting of melanopsin-expressing RGCs to the IPL. In Sema5A-/- and Sema5B-/- mice the RGCs exhibit aberrant dendritic branching in INL, OPL and ONL (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F10/?report=objectonly" target="object" rid-figpopup="figNingRGCDF10" rid-ob="figobNingRGCDF10">Fig. 10B, 10C and 10G</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF10" co-legend-rid="figlgndNingRGCDF10"><a href="/books/NBK100303/figure/NingRGCD.F10/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF10" rid-ob="figobNingRGCDF10"><img class="small-thumb" src="/books/NBK100303/bin/Figure_10.gif" src-large="/books/NBK100303/bin/Figure_10.jpg" alt="Figure 10" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF10"><h4 id="NingRGCD.F10"><a href="/books/NBK100303/figure/NingRGCD.F10/?report=objectonly" target="object" rid-ob="figobNingRGCDF10">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 10. Sema5A and Sema5B constrain dendritic targeting of RGCs to the IPL. WT; Thy-1:GFP-M (A) and Sema5A-/-; Sema5B-/-; Thy-1:GFP-M (B and C) adult retina sections were immunostained with anti-GFP or WT (E) and Sema5A-/-; Sema5B-/- (F and G) adult <a href="/books/NBK100303/figure/NingRGCD.F10/?report=objectonly" target="object" rid-ob="figobNingRGCDF10">(more...)</a></p></div></div><p>Several reports have also shown that both spontaneous synaptic activity mediated by glutamate receptor (GluR) before eye opening and light evoked retinal activity after eye opening regulate the normal development of the lamina-restricted dendritic patterns of RGCs. In an early developing vertebrate retina like mouse, RGCs fire periodic bursts of action potentials that are highly correlated and propagate across the RGC layer in a wave-like fashion (<a class="bk_pop" href="#NingRGCD.REF.39">39</a>). These spontaneous retinal waves are mainly mediated by cholinergic and glutamatergic synaptic transmission (<a class="bk_pop" href="#NingRGCD.REF.40" data-bk-pop-others="NingRGCD.REF.41 NingRGCD.REF.42 NingRGCD.REF.43 NingRGCD.REF.44 NingRGCD.REF.45">40-45</a>) (see chapter by <a href="/books/n/webvision/ch21dev2/">Ford and Feller, Webvision</a>). The retinal wave mediated by AChR seems to have little effect on the formation of laminar-restricted dendritic pattern of RGCs. In mice, genetic deletion of β2 subunits of nAChR or the sole synthetic enzyme for acetylcholine, choline acetyltransferase, eliminates the retinal waves mediated by nAChRs and causes an insignificant or non detectable change of the development of the lamina-restricted dendritic ramification of RGCs (<a class="bk_pop" href="#NingRGCD.REF.40" data-bk-pop-others="NingRGCD.REF.46">40, 46</a>).</p><p>On the other hand, intraocular injection of APB, an agonist for class III metabotropic GluRs (mGluR6), results in a blockade of glutamate release from ON and rod bipolar cells and causes an arrest of the developmental stratification and segregation of RGC dendrites into ON and OFF synaptic pathways in cats, ferrets and rats (<a class="bk_pop" href="#NingRGCD.REF.29" data-bk-pop-others="NingRGCD.REF.30 NingRGCD.REF.47 NingRGCD.REF.48">29, 30, 47, 48</a>) (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F11/?report=objectonly" target="object" rid-figpopup="figNingRGCDF11" rid-ob="figobNingRGCDF11">Fig 11</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF11" co-legend-rid="figlgndNingRGCDF11"><a href="/books/NBK100303/figure/NingRGCD.F11/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF11" rid-ob="figobNingRGCDF11"><img class="small-thumb" src="/books/NBK100303/bin/Figure_11.gif" src-large="/books/NBK100303/bin/Figure_11.jpg" alt="Figure 11" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF11"><h4 id="NingRGCD.F11"><a href="/books/NBK100303/figure/NingRGCD.F11/?report=objectonly" target="object" rid-ob="figobNingRGCDF11">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 11. Glutamate released from bipolar cells regulates the dendritic development of RGCs. A, B and C: Light micrographs of DiI labeled RGCs from sections of a P2, a P10 and an APB-treated P10 cat retina, respectively. At P2 the RGC dendrites are distributed <a href="/books/NBK100303/figure/NingRGCD.F11/?report=objectonly" target="object" rid-ob="figobNingRGCDF11">(more...)</a></p></div></div><p>Also, intraocular injection of antagonists for NMDA and AMPA receptors, AP5 and NBQX, increases the density of filopodia by more than 100% after 5 days of treatment in mice (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F12/?report=objectonly" target="object" rid-figpopup="figNingRGCDF12" rid-ob="figobNingRGCDF12">see Fig 12, compare A and B</a>). Xu et al. (<a class="bk_pop" href="#NingRGCD.REF.44">44</a>) showed that pharmacological blockade of GluR-mediated activity slows the kinetics of RGC dendritic growth and elimination by approximately 50% <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F12/?report=objectonly" target="object" rid-figpopup="figNingRGCDF12" rid-ob="figobNingRGCDF12">(Fig. 12D</a>). The disrupted GluR-mediated activity in retina during early postnatal development is associated with profound and permanent defects of RGC dendritic morphology and synaptic function in adults (<a class="bk_pop" href="#NingRGCD.REF.44">44</a>). Similarly, Lau et al. (<a class="bk_pop" href="#NingRGCD.REF.49">49</a>) showed that blockade of NMDA receptors before eye opening increases the spine density of RGCs in hamsters.</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF12" co-legend-rid="figlgndNingRGCDF12"><a href="/books/NBK100303/figure/NingRGCD.F12/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF12" rid-ob="figobNingRGCDF12"><img class="small-thumb" src="/books/NBK100303/bin/Figure_12.gif" src-large="/books/NBK100303/bin/Figure_12.jpg" alt="Figure 12" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF12"><h4 id="NingRGCD.F12"><a href="/books/NBK100303/figure/NingRGCD.F12/?report=objectonly" target="object" rid-ob="figobNingRGCDF12">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 12. GluR-mediated activity regulates the dendritic development of RGCs. A and B: Representative images and dendritic reconstructions of YFP-expressing RGCs of P12 retinas in control and with intraocular treatment of NBQX+AP5. Note that NBQX+AP5 <a href="/books/NBK100303/figure/NingRGCD.F12/?report=objectonly" target="object" rid-ob="figobNingRGCDF12">(more...)</a></p></div></div><p>However, genetic blockade of glutamate release from ON bipolar cells eliminates spontaneous and light evoked synaptic inputs to ON RGCs without effect on the spontaneous and light evoked synaptic activity of OFF RGCs and causes no detectable effect on the lamina-restricted dendritic ramification of either ON or OFF RGCs (<a class="bk_pop" href="#NingRGCD.REF.50">50</a>). In addition, genetic deletion of the mGluR6 receptor, which blocks ON bipolar cell light evoked synaptic activity, failed to impair dendritic stratification of mouse RGCs (<a class="bk_pop" href="#NingRGCD.REF.51">51</a>). Therefore, the effect of GluR-mediated synaptic activity on the development of the lamina-restricted dendritic ramification and synaptic connections of RGCs is somewhat controversial and needs to be further investigated. The effect of light evoked synaptic activity on the development of RGC dendritic restriction and synaptic connection seems to vary among subtypes of RGCs and selective to some synaptic features. Morphologically, dark rearing blocks an age-dependent remodeling of dendritic complexity of a class of “aberrant” RGCs in hamster retina (<a class="bk_pop" href="#NingRGCD.REF.52">52</a>). In mice, light deprivation increases the density of conventional synapses in the IPL (<a class="bk_pop" href="#NingRGCD.REF.53">53</a>). The developmental ramification of RGC dendrites into OFF lamina of the IPL is selectively impaired by light deprivation in RGCs of mouse retina (<a class="bk_pop" href="#NingRGCD.REF.54">54</a>). Functionally, light deprivation blocks the surge of spontaneous synaptic inputs to RGCs, the age-dependent increase of inner retinal light responses measured by ERG oscillatory potentials (<a class="bk_pop" href="#NingRGCD.REF.55" data-bk-pop-others="NingRGCD.REF.56">55, 56</a>), the segregation of RGC synaptic inputs from ON and OFF synaptic pathways (<a class="bk_pop" href="#NingRGCD.REF.54">54</a>), and the maturation of the size of inhibitory receptive field of RGCs (<a class="bk_pop" href="#NingRGCD.REF.57">57</a>).</p><p>However, light deprivation seems preferentially to affect the maturation of dendrites of OFF RGCs, but not ON RGCs. Xu and Tian (<a class="bk_pop" href="#NingRGCD.REF.54">54</a>) quantitatively analyzed the developmental refinement of the dendrites of a random group of RGCs in mouse retina and determined the ramification depth and width of RGC dendrites in the IPL at different postnatal ages (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F13/?report=objectonly" target="object" rid-figpopup="figNingRGCDF13" rid-ob="figobNingRGCDF13">Fig. 13</a>). They showed that a large proportion of RGCs have a single layer of narrowly stratified dendritic plexus ramifying near the centre of the IPL before eye opening (P12), where they could synapse with both ON and OFF bipolar cells. After eye opening, a significant portion of RGCs redistribute their dendrites from the centre of the IPL toward the inner and outer borders of the IPL (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-figpopup="figNingRGCDF14" rid-ob="figobNingRGCDF14">Fig. 14A</a>). This laminar-specific redistribution of RGC dendrites is associated with an age-dependent decrease of the number of RGCs receiving synaptic inputs from both ON and OFF bipolar cells <a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-figpopup="figNingRGCDF14" rid-ob="figobNingRGCDF14">(Fig. 14C</a>). In dark reared mice, the RGC dendritic redistribution from the centre of the IPL to sublamina a of the IPL is blocked, which results in a significant increase of the number of RGCs ramifying at the center of the IPL, and a decrease of the number of RGCs ramifying only in sublamina a, in comparison with age-matched controls (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-figpopup="figNingRGCDF14" rid-ob="figobNingRGCDF14">Fig. 14A</a>). Physiologically, the number of RGCs responding to both the onset and the offset of light stimulation of mice raised in constant darkness from birth to the ages of P27-30 was 4-fold higher than that of age-matched controls raised in cyclic light, but comparable to the percentage of ON-OFF responsive RGCs of P10-12 mice (<a class="bk_pop" href="#NingRGCD.REF.58">58</a>) (<a class="figpopup" href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-figpopup="figNingRGCDF14" rid-ob="figobNingRGCDF14">Fig. 14C</a>). Similarly, long-term treatment of cat eyes with intraocular injection of APB significantly reduced the number of αRGCs ramifying in the sublamina a and increased the number of multistratified α cells (<a class="bk_pop" href="#NingRGCD.REF.48">48</a>).</p><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF13" co-legend-rid="figlgndNingRGCDF13"><a href="/books/NBK100303/figure/NingRGCD.F13/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF13" rid-ob="figobNingRGCDF13"><img class="small-thumb" src="/books/NBK100303/bin/Figure_13.gif" src-large="/books/NBK100303/bin/Figure_13.jpg" alt="Figure 13" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF13"><h4 id="NingRGCD.F13"><a href="/books/NBK100303/figure/NingRGCD.F13/?report=objectonly" target="object" rid-ob="figobNingRGCDF13">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 13. RGC dendritic distribution in the IPL can be quantified. The dendritic distribution of YFP-expressing RGCs in the IPL was quantified from confocal images Thy1-YFP mice. A: A stacked image (A1), the 90° rotation view (A2) and the quantitative <a href="/books/NBK100303/figure/NingRGCD.F13/?report=objectonly" target="object" rid-ob="figobNingRGCDF13">(more...)</a></p></div></div><div class="iconblock whole_rhythm clearfix ten_col fig" id="figNingRGCDF14" co-legend-rid="figlgndNingRGCDF14"><a href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" title="Figure" class="img_link icnblk_img figpopup" rid-figpopup="figNingRGCDF14" rid-ob="figobNingRGCDF14"><img class="small-thumb" src="/books/NBK100303/bin/NingFig14color.gif" src-large="/books/NBK100303/bin/NingFig14color.jpg" alt="Figure 14" /></a><div class="icnblk_cntnt" id="figlgndNingRGCDF14"><h4 id="NingRGCD.F14"><a href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-ob="figobNingRGCDF14">Figure</a></h4><p class="float-caption no_bottom_margin">Figure 14. Light deprivation alters the dendritic ramification and synaptic inputs of mouse RGCs. A: Peak dendritic location of all mono-stratified RGCs of P12, P33 and P33 dark-reared mice. Note that the number of RGC with peak located near 30% of the <a href="/books/NBK100303/figure/NingRGCD.F14/?report=objectonly" target="object" rid-ob="figobNingRGCDF14">(more...)</a></p></div></div></div><div id="NingRGCD.5_The_possible_mechanisms_of_de"><h2 id="_NingRGCD_5_The_possible_mechanisms_of_de_">5. The possible mechanisms of developmental regulation of RGC dendrites</h2><p>During developmental refinement, the dendritic arborizations of RGCs undergo dynamic elaboration, maintenance or elimination to attain their lamina-restricted ramification pattern. Although neuronal activity influences this remodeling in many subtypes, the underlying molecular mechanisms have not yet been identified. Several studies suggest that calcium is important to link the neuronal activity with dendritic growth and patterning (<a class="bk_pop" href="#NingRGCD.REF.59">59</a>). Thus, it has been reported that synaptic stimulation induces calcium influx through voltage-dependent calcium channels and is sufficient to activate a transcriptional program that regulates dendritic growth (<a class="bk_pop" href="#NingRGCD.REF.60">60</a>).</p><p>BDNF/TrkB has also been shown to play an essential role in the activity-dependent development of RGC dendrites (<a class="bk_pop" href="#NingRGCD.REF.61">61</a>). Activation of BDNF promotes the anatomical segregation of the dendrites of ON- and OFF-center RGCs in different sublaminae of the IPL (<a class="bk_pop" href="#NingRGCD.REF.61" data-bk-pop-others="NingRGCD.REF.62">61, 62</a>), while deletion of TrkB strongly inhibits visual experience-dependent refinement of RGC dendrites (<a class="bk_pop" href="#NingRGCD.REF.62">62</a>). In addition, the expression of BDNF in the retina is up-regulated by visual stimulation (<a class="bk_pop" href="#NingRGCD.REF.61" data-bk-pop-others="NingRGCD.REF.63 NingRGCD.REF.64 NingRGCD.REF.65">61, 63-65</a>). This suggests that light deprivation retards RGC dendritic maturation by reduction of the expression of BDNF. Conversely, over-expression of BDNF precludes the retardation of laminar refinement in dark reared mice (<a class="bk_pop" href="#NingRGCD.REF.62">62</a>).</p><p>Recent studies demonstrated that genes typically associated with the immune system, such as those in the major histocompatibility complex (MHC), are expressed by neurons in various regions of the CNS, including retina, and play important roles in synapse formation and activity-dependent synaptic plasticity (<a class="bk_pop" href="#NingRGCD.REF.66" data-bk-pop-others="NingRGCD.REF.67 NingRGCD.REF.68 NingRGCD.REF.69 NingRGCD.REF.70 NingRGCD.REF.71 NingRGCD.REF.72">66-72</a>). Genetic deletion or mutation of a number of MHC class I genes result in the failure of eye-specific segregation of RGC axon projections to the dosal lateral geniculat nucleus (dLGN) (<a class="bk_pop" href="#NingRGCD.REF.68" data-bk-pop-others="NingRGCD.REF.72">68, 72</a>). Also, long-term potentiation, long-term depression, learning, memory, and neurogenesis in hippocampus are impaired (<a class="bk_pop" href="#NingRGCD.REF.68" data-bk-pop-others="NingRGCD.REF.73">68, 73</a>).</p><p>Xu et al. (<a class="bk_pop" href="#NingRGCD.REF.44">44</a>) reported that the key component of MHCI receptor, CD3ζ is specifically expressed by RGCs in mouse retina. Similar to the pharmacological blockade of GluR-mediated activity, genetic mutation of CD3ζ profoundly reduces the kinetics of RGC dendritic growth and pruning, and impairs the lamina-specific segregation of RGC dendrites in the IPL. In addition, CD3ζ-/- mice show a selective reduction of GluR-mediated synaptic transmission in RGCs suggesting that CD3ζ-mediated signaling participates in activity-dependent synaptic maturation of RGCs. However, some of the important questions, such as what are the exact molecule mechanisms with which activation of MHC/CD3ζ on neurons affects the maturation of RGC dendrites, and how MHC/CD3ζ-mediated signaling interacts with neurotransmitter-mediated synaptic activity in dendritic maturation, need to be further addressed.</p></div><div id="NingRGCD.About_the_Author"><h2 id="_NingRGCD_About_the_Author_">About the Author</h2><p>
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<span class="graphic"><img src="/books/NBK100303/bin/NingTian.jpg" alt="Image NingTian.jpg" /></span>
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</p><p>Dr. Ning Tian was initially trained as a physician in China (Yichang Medical School) and then received his Master Degree in clinical visual physiology from Zhong-sen Ophthalmic Center, Sun Yat-sen University of Medical Sciences, China. He practiced clinical ophthalmology for a while before doing a PhD in Biophysics and Physiology at the State University of New York at Buffalo with Dr. Malcolm Slaughter. Ning then did a postdoc with Dr. David Copenhagen at University of California, San Francisco. After being an Assistant Research Ophthalmologist at the University of California, San Francisco from 1998-2000, he headed a laboratory at Yale University (2000-2009). Ning is presently an Associate Professor of Ophthalmology and Neurobiology in the Moran Eye Center, University of Utah. His research is focused on understanding the cellular and molecular mechanisms that regulate the maturation of retinal ganglion cell synaptic function and dendritic structure.</p></div><div id="NingRGCD.References"><h2 id="_NingRGCD_References_">References</h2><dl class="temp-labeled-list"><dt>1.</dt><dd><div class="bk_ref" id="NingRGCD.REF.1">Famiglietti E.V. Jr, Kolb H.
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<em>Structural basis for ON-and OFF-center responses in retinal ganglion cells.</em>
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<em>Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in the cat retina.</em>
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<span><span class="ref-journal">J. Neurophysiol. </span>1978;<span class="ref-vol">41</span>(2):472–483.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/650277" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 650277</span></a>]</div></dd><dt>3.</dt><dd><div class="bk_ref" id="NingRGCD.REF.3">Schiller P.H.
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<em>Parallel information processing channels created in the retina.</em>
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<span><span class="ref-journal">Proc Natl Acad Sci U S A. </span>2010;<span class="ref-vol">107</span>(40):17087–94.</span> [<a href="/pmc/articles/PMC2951406/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC2951406</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/20876118" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 20876118</span></a>]</div></dd><dt>4.</dt><dd><div class="bk_ref" id="NingRGCD.REF.4">Euler T., Wassle H.
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<em>Immunocytochemical identification of cone bipolar cells in the rat retina.</em>
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<span><span class="ref-journal">J Comp Neurol. </span>1995;<span class="ref-vol">361</span>(3):461–78.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/8550893" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 8550893</span></a>]</div></dd><dt>5.</dt><dd><div class="bk_ref" id="NingRGCD.REF.5">MacNeil M.A., Masland R.H.
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<em>Extreme diversity among amacrine cells: implications for function.</em>
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<span><span class="ref-journal">Neuron. </span>1998;<span class="ref-vol">20</span>(5):971–82.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/9620701" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 9620701</span></a>]</div></dd><dt>6.</dt><dd><div class="bk_ref" id="NingRGCD.REF.6">Ghosh K.K. et al.
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<em>Types of bipolar cells in the mouse retina.</em>
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<span><span class="ref-journal">J Comp Neurol. </span>2004;<span class="ref-vol">469</span>(1):70–82.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/14689473" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 14689473</span></a>]</div></dd><dt>7.</dt><dd><div class="bk_ref" id="NingRGCD.REF.7">. J., C. and L.M. Chalupa, <em>Morphological, functional, and developmental properties of mouse retinal ganglion cells.</em>, in <em>Eye, retina, and visual system of the mouse</em>, L.M. Chalupa and R.W. Williams, Editors. 2008, MIT Press: Cambridge, Mass. p. 189-199.</div></dd><dt>8.</dt><dd><div class="bk_ref" id="NingRGCD.REF.8">Kuffler S.W.
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<em>Discharge patterns and functional organization of mammalian retina.</em>
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<span><span class="ref-journal">J Neurophysiol. </span>1953;<span class="ref-vol">16</span>(1):37–68.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/13035466" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 13035466</span></a>]</div></dd><dt>9.</dt><dd><div class="bk_ref" id="NingRGCD.REF.9">Masland R.H.
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<em>The fundamental plan of the retina.</em>
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<span><span class="ref-journal">Nat Neurosci. </span>2001;<span class="ref-vol">4</span>(9):877–86.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/11528418" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 11528418</span></a>]</div></dd><dt>10.</dt><dd><div class="bk_ref" id="NingRGCD.REF.10">Wässle H.
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<em>Parallel processing in the mammalian retina.</em>
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<span><span class="ref-journal">Nat Rev Neurosci. </span>2004;<span class="ref-vol">5</span>(10):747–57.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/15378035" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 15378035</span></a>]</div></dd><dt>11.</dt><dd><div class="bk_ref" id="NingRGCD.REF.11">Badea T.C., Nathans J.
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<em>Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter.</em>
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<span><span class="ref-journal">J Comp Neurol. </span>2004;<span class="ref-vol">480</span>(4):331–51.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/15558785" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 15558785</span></a>]</div></dd><dt>12.</dt><dd><div class="bk_ref" id="NingRGCD.REF.12">Berson, D.M., <em>Retinal ganglion cell types and their central projections.</em>, Volume 1, in <em>The senses : a comprehensive reference</em>, A.I. Basbaum, et al., Editors. 2008, Elsevier: Amsterdam; Boston. p. 491–520.</div></dd><dt>13.</dt><dd><div class="bk_ref" id="NingRGCD.REF.13">Coombs J. et al.
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<em>Morphological properties of mouse retinal ganglion cells.</em>
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<span><span class="ref-journal">Neuroscience. </span>2006;<span class="ref-vol">140</span>(1):123–36.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/16626866" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 16626866</span></a>]</div></dd><dt>14.</dt><dd><div class="bk_ref" id="NingRGCD.REF.14">Dacey D.M., Packer O.S.
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<em>Colour coding in the primate retina: diverse cell types and cone-specific circuitry.</em>
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<span><span class="ref-journal">Proc Natl Acad Sci U S A. </span>2003;<span class="ref-vol">100</span>(22):13048–53.</span> [<a href="/pmc/articles/PMC240742/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC240742</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/14569018" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 14569018</span></a>]</div></dd><dt>72.</dt><dd><div class="bk_ref" id="NingRGCD.REF.72">Xu, Y. and N. Vardi, <em>Modulation of the Light-Activated Cation Channel in Retinal ON Bipolar Cells by G-Protein Subunits.</em> ARVO Meeting Abstracts, 2010<strong>51</strong>(5): p. 4797.</div></dd><dt>73.</dt><dd><div class="bk_ref" id="NingRGCD.REF.73">Ziv Y. et al.
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<em>Neurons of the human retina: a Golgi study.</em>
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<em>Cell differentiation in the retina of the mouse.</em>
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<em>Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina.</em>
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<em>Pathway-specific maturation, visual deprivation, and development of retinal pathway.</em>
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<span><span class="ref-journal">Neuroscientist. </span>2004;<span class="ref-vol">10</span>(4):337–46.</span> [<a href="https://pubmed.ncbi.nlm.nih.gov/15271261" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 15271261</span></a>]</div></dd><dt>80.</dt><dd><div class="bk_ref" id="NingRGCD.REF.80">Matsuoka R.L. et al.
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<em>Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function.</em>
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<span><span class="ref-journal">Neuron. </span>2011;<span class="ref-vol">71</span>(3):460–73.</span> [<a href="/pmc/articles/PMC3164552/" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pmc">PMC free article<span class="bk_prnt">: PMC3164552</span></a>] [<a href="https://pubmed.ncbi.nlm.nih.gov/21835343" ref="pagearea=cite-ref&targetsite=entrez&targetcat=link&targettype=pubmed">PubMed<span class="bk_prnt">: 21835343</span></a>]</div></dd></dl></div><div id="bk_toc_contnr"></div></div></div>
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<div class="post-content"><div><div class="half_rhythm"><a href="/books/about/copyright/">Copyright</a>: © 2025 Webvision .<p class="small">All copyright for chapters belongs to the individual authors who created them. However, for non-commercial, academic purposes, images and content from the chapters portion of Webvision may be used with a non-exclusive rights under a Attribution, <a href="https://creativecommons.org/licenses/by-nc/4.0/" ref="pagearea=meta&targetsite=external&targetcat=link&targettype=uri">Noncommercial 4.0 International (CC BY-NC) Creative Commons license</a>. Cite Webvision, http://webvision.med.utah.edu/ as the source. Commercial applications need to obtain license permission from the administrator of Webvision and are generally declined unless the copyright owner can/wants to donate or license material. Use online should be accompanied by a link back to the original source of the material. All imagery or content associated with blog posts belong to the authors of said posts, except where otherwise noted.</p></div><div class="small"><span class="label">Bookshelf ID: NBK100303</span><span class="label">PMID: <a href="https://pubmed.ncbi.nlm.nih.gov/22953362" title="PubMed record of this page" ref="pagearea=meta&targetsite=entrez&targetcat=link&targettype=pubmed">22953362</a></span></div><div style="margin-top:2em" class="bk_noprnt"><a class="bk_cntns" href="/books/n/webvision/">Contents</a><div class="pagination bk_noprnt"><a class="active page_link prev" href="/books/n/webvision/ch21dev2/" title="Previous page in this title">< Prev</a><a class="active page_link next" href="/books/n/webvision/colorpercep/" title="Next page in this title">Next ></a></div></div></div></div>
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<div xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance"></div><div class="portlet"><div class="portlet_head"><div class="portlet_title"><h3><span>Views</span></h3></div><a name="Shutter" sid="1" href="#" class="portlet_shutter" title="Show/hide content" remembercollapsed="true" pgsec_name="PDF_download" id="Shutter"></a></div><div class="portlet_content"><ul xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="simple-list"><li><a href="/books/NBK100303/?report=reader">PubReader</a></li><li><a href="/books/NBK100303/?report=printable">Print View</a></li><li><a data-jig="ncbidialog" href="#_ncbi_dlg_citbx_NBK100303" data-jigconfig="width:400,modal:true">Cite this Page</a><div id="_ncbi_dlg_citbx_NBK100303" style="display:none" title="Cite this Page"><div class="bk_tt">Tian N. Development of Retinal Ganglion Cell Dendritic Structure and Synaptic Connections. 2012 Jun 13. In: Kolb H, Fernandez E, Jones B, et al., editors. Webvision: The Organization of the Retina and Visual System [Internet]. Salt Lake City (UT): University of Utah Health Sciences Center; 1995-. <span class="bk_cite_avail"></span></div></div></li><li><a href="/books/NBK100303/pdf/Bookshelf_NBK100303.pdf">PDF version of this page</a> (2.5M)</li><li><a href="/books/n/webvision/pdf/">PDF version of this title</a> (235M)</li></ul></div></div><div class="portlet"><div class="portlet_head"><div class="portlet_title"><h3><span>In this Page</span></h3></div><a name="Shutter" sid="1" href="#" class="portlet_shutter" title="Show/hide content" remembercollapsed="true" pgsec_name="page-toc" id="Shutter"></a></div><div class="portlet_content"><ul xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="simple-list"><li><a href="#NingRGCD.1_Introduction" ref="log$=inpage&link_id=inpage">Introduction</a></li><li><a href="#NingRGCD.2_Neurogenesis_and_synaptogenes" ref="log$=inpage&link_id=inpage">Neurogenesis and synaptogenesis of retina</a></li><li><a href="#NingRGCD.3_Formation_of_laminarestricted" ref="log$=inpage&link_id=inpage"> Formation of lamina-restricted dendritic distributions of RGCs</a></li><li><a href="#NingRGCD.4_Regulation_of_the_formation_o" ref="log$=inpage&link_id=inpage"> Regulation of the formation of lamina-restricted dendritic patterns of RGCs</a></li><li><a href="#NingRGCD.5_The_possible_mechanisms_of_de" ref="log$=inpage&link_id=inpage"> The possible mechanisms of developmental regulation of RGC dendrites</a></li><li><a href="#NingRGCD.About_the_Author" ref="log$=inpage&link_id=inpage">About the Author</a></li><li><a href="#NingRGCD.References" ref="log$=inpage&link_id=inpage">References</a></li></ul></div></div><div class="portlet"><div class="portlet_head"><div class="portlet_title"><h3><span>Related Items in Bookshelf</span></h3></div><a name="Shutter" sid="1" href="#" class="portlet_shutter" title="Show/hide content" remembercollapsed="true" pgsec_name="source-links" id="Shutter"></a></div><div 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xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="invert">Review</span> Bipolar Cell Pathways in the Vertebrate Retina.</a><span class="source">[Webvision: The Organization of...]</span><div class="brieflinkpop offscreen_noflow"><span xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="invert">Review</span> Bipolar Cell Pathways in the Vertebrate Retina.<div class="brieflinkpopdesc"><em xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="author">Nelson R, Connaughton V. </em><em xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="cit">Webvision: The Organization of the Retina and Visual System. 1995</em></div></div></li><li class="brieflinkpopper two_line"><a class="brieflinkpopperctrl" href="/pubmed/32119275" 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Epub 2024 Dec 24.</em></div></div></li><li class="brieflinkpopper two_line"><a class="brieflinkpopperctrl" href="/pubmed/36137063" ref="ordinalpos=1&linkpos=5&log$=relatedreviews&logdbfrom=pubmed"><span xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="invert">Review</span> Depressing time: Waiting, melancholia, and the psychoanalytic practice of care.</a><span class="source">[The Time of Anthropology: Stud...]</span><div class="brieflinkpop offscreen_noflow"><span xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="invert">Review</span> Depressing time: Waiting, melancholia, and the psychoanalytic practice of care.<div class="brieflinkpopdesc"><em xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="author">Salisbury L, Baraitser L. </em><em xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" class="cit">The Time of Anthropology: Studies of Contemporary Chronopolitics. 2020</em></div></div></li></ul><a class="seemore" href="/sites/entrez?db=pubmed&cmd=link&linkname=pubmed_pubmed_reviews&uid=22953362" ref="ordinalpos=1&log$=relatedreviews_seeall&logdbfrom=pubmed">See reviews...</a><a class="seemore" href="/sites/entrez?db=pubmed&cmd=link&linkname=pubmed_pubmed&uid=22953362" ref="ordinalpos=1&log$=relatedarticles_seeall&logdbfrom=pubmed">See all...</a></div></div><div class="portlet"><div class="portlet_head"><div class="portlet_title"><h3><span>Recent Activity</span></h3></div><a name="Shutter" sid="1" href="#" class="portlet_shutter" title="Show/hide content" remembercollapsed="true" pgsec_name="recent_activity" id="Shutter"></a></div><div class="portlet_content"><div xmlns:np="http://ncbi.gov/portal/XSLT/namespace" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" id="HTDisplay" class=""><div class="action"><a href="javascript:historyDisplayState('ClearHT')">Clear</a><a href="javascript:historyDisplayState('HTOff')" class="HTOn">Turn Off</a><a href="javascript:historyDisplayState('HTOn')" class="HTOff">Turn On</a></div><ul id="activity"><li class="ra_rcd ralinkpopper two_line"><a class="htb ralinkpopperctrl" ref="log$=activity&linkpos=1" href="/portal/utils/pageresolver.fcgi?recordid=67c9a757f4a390645ea44f7b">Development of Retinal Ganglion Cell Dendritic Structure and Synaptic Connection...</a><div class="ralinkpop offscreen_noflow">Development of Retinal Ganglion Cell Dendritic Structure and Synaptic Connections - Webvision<div class="brieflinkpopdesc"></div></div><div class="tertiary"></div></li><li class="ra_rcd ralinkpopper two_line"><a class="htb ralinkpopperctrl" ref="log$=activity&linkpos=2" href="/portal/utils/pageresolver.fcgi?recordid=67c9a756f4a390645ea44a0b">Formation of Early Retinal Circuits in the Inner-Plexiform Layer - Webvision</a><div class="ralinkpop offscreen_noflow">Formation of Early Retinal Circuits in the Inner-Plexiform Layer - Webvision<div class="brieflinkpopdesc"></div></div><div class="tertiary"></div></li><li class="ra_rcd ralinkpopper two_line"><a class="htb ralinkpopperctrl" ref="log$=activity&linkpos=3" href="/portal/utils/pageresolver.fcgi?recordid=67c9a755b15b832ebc793966">Development of cell types and synaptic connections in the retina by Josh Morgan ...</a><div class="ralinkpop offscreen_noflow">Development of cell types and synaptic connections in the retina by Josh Morgan and Rachel Wong - Webvision<div class="brieflinkpopdesc"></div></div><div class="tertiary"></div></li><li class="ra_rcd ralinkpopper two_line"><a class="htb ralinkpopperctrl" ref="log$=activity&linkpos=4" href="/portal/utils/pageresolver.fcgi?recordid=67c9a753f4a390645ea434db">Part VI: Retinal Neurogenesis: Early stages in the development of neurons and pa...</a><div class="ralinkpop offscreen_noflow">Part VI: Retinal Neurogenesis: Early stages in the development of neurons and pathways - Webvision<div class="brieflinkpopdesc"></div></div><div class="tertiary"></div></li><li class="ra_rcd ralinkpopper two_line"><a class="htb ralinkpopperctrl" ref="log$=activity&linkpos=5" href="/portal/utils/pageresolver.fcgi?recordid=67c9a752b15b832ebc79270f">S-Potentials and Horizontal Cells - Webvision</a><div class="ralinkpop offscreen_noflow">S-Potentials and Horizontal Cells - Webvision<div class="brieflinkpopdesc"></div></div><div class="tertiary"></div></li></ul><p class="HTOn">Your browsing activity is empty.</p><p class="HTOff">Activity recording is turned off.</p><p id="turnOn" class="HTOff"><a href="javascript:historyDisplayState('HTOn')">Turn recording back on</a></p><a class="seemore" href="/sites/myncbi/recentactivity">See more...</a></div></div></div>
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