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Expressing Ganglion Cells on Macaque and Human Retinas Form Two Morphologically Distinct Populations

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Expressing Ganglion Cells on Macaque and Human Retinas Form Two Morphologically Distinct Populations RESEARCH ARTICLE Melanopsin-Expressing Ganglion Cells on Macaque and Human Retinas Form Two Morphologically Distinct Populations Hsi-Wen Liao,1 Xiaozhi Ren,1 Beth B. Peterson,2 David W. Marshak,3 King-Wai Yau,1,4 Paul D. Gamlin,5 and Dennis M. Dacey2* 1Department of Neuroscience, John Hopkins University School of Medicine, Baltimore, Maryland 21205-2185 2Department of Biological Structure, University of Washington and the Washington National Primate Research Center, Seattle, Washington 98195-7420 3Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas 77030 4Department of Ophthalmology, John Hopkins University School of Medicine, Baltimore, Maryland 21205-2185 5Department of Ophthalmology, University of Alabama at Birmingham, Birmingham, Alabama 35294 ABSTRACT inputs from DB6 bipolar cells via a sparse outer axonal The long-term goal of this research is to understand arbor. Outer stratifying melanopsin cells also received how retinal ganglion cells that express the photopig- inputs from axon terminals of dopaminergic amacrine ment melanopsin, also known as OPN4, contribute to cells. On the outer stratifying melanopsin cells, ribbon vision in humans and other primates. Here we report synapses from bipolar cells and conventional synapses the results of anatomical studies using our polyclonal from amacrine cells were identified in electron micro- antibody specifically against human melanopsin that scopic immunolabeling experiments. Both inner and confirm and extend previous descriptions of melanopsin outer stratifying melanopsin cell types were retro- cells in primates. In macaque and human retina, two gradely labeled following tracer injection in the lateral distinct populations of melanopsin cells were identified geniculate nucleus (LGN). In addition, a method for tar- based on dendritic stratification in either the inner or geting melanopsin cells for intracellular injection using the outer portion of the inner plexiform layer (IPL). Vari- their intrinsic fluorescence was developed. This tech- ation in dendritic field size and cell density with eccen- nique was used to demonstrate that melanopsin cells tricity was confirmed, and dendritic spines, a new were tracer coupled to amacrine cells and would be feature of melanopsin cells, were described. The spines applicable to electrophysiological experiments in the were the sites of input from DB6 diffuse bipolar cell future. J. Comp. Neurol. 000:000–000, 2016. axon terminals to the inner stratifying type of melanop- VC 2016 The Authors The Journal of Comparative Neurology Published by sin cells. The outer stratifying melanopsin type received Wiley Periodicals, Inc. INDEXING TERMS: primate retina; intrinsically photosensitive ganglion cell; dopamine; bipolar cell; amacrine cell; RRID:AB_397181 Retinal ganglion cells that express the photopigment This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and dis- melanopsin and generate responses to light without requir- tribution in any medium, provided the original work is properly cited, the ing any synaptic input from other retinal neurons were first use is non-commercial and no modifications or adaptations are made. Grant sponsor: National Eye Institute; Grant numbers: #EY06678 (to described from rodent retinas (Provencio et al., 2000; D.M.D.) #EY09625 (to D.M.D.) #EY06837 (to K.-W.Y.) EY14596 (to K.- Berson et al., 2002). The responses mediated by the W.Y.); Grant sponsor: National Institute of Neurological Diseases and Stroke Project 4; Grant numbers: NS38310 (to D.M.D.); EY09380 (to photopigment were relatively insensitive to light and had P.D.G.); EY10608 (to D.W.M., D.M.D., P.D.G.); EY01730 (to D.W.M., slow kinetics, beginning after a long delay and outlasting D.M.D., P.D.G.); EY03039 (to D.W.M., D.M.D., P.D.G.); Grant sponsor: Retina Research Foundation Paul Kayser Award (to D.M.D.). the stimulus. These intrinsically photosensitive ganglion *CORRESPONDENCE TO: Dennis M. Dacey, Department of Biological cells project to the hypothalamus, where they provide Structure, University of Washington, Seattle, WA 98195. E-mail: dmd@u. washington.edu the visual input to synchronize the master circadian clock Received July 10, 2015; Revised January 30, 2016; in the brain with the daily changes in illumination. These Accepted March 7, 2016. DOI 10.1002/cne.23995 VC 2016 The Authors The Journal of Comparative Neurology Published by Published online Month 00, 2016 in Wiley Online Library Wiley Periodicals, Inc. (wileyonlinelibrary.com) The Journal of Comparative Neurology | Research in Systems Neuroscience 00:00–00 (2016) 1 H.-W. Liao et al. ganglion cells also project to the pretectum, where they (Dkhissi-Benyahya et al., 2006; La Morgia et al., 2010; provide input to the neurons that control the diameter of Neumann et al., 2011). the pupil, and to other nuclei in the brainstem (Hattar Some of the synaptic inputs to melanopsin ganglion et al., 2002). Initially, most of the research on intrinsi- cells of primates have been described by using light cally photosensitive ganglion cells dealt with their roles microscopic, immunolabeling techniques. In marmosets, in visual functions that do not require formation of melanopsin cells received inputs from both bipolar cells images. More recent studies indicate that melanopsin and amacrine cells (Jusuf et al., 2007). DB6 diffuse bipo- ganglion cells also project to targets within the retina lar cells, which are presumed to have ON responses to and contribute to conscious perception of light in light in their receptive field centers based on their mor- humans and to image formation in other mammals (Do phology, provided input to inner stratifying melanopsin and Yau, 2010; Lucas, 2013). cells via their axon terminals. The axons of DB6 bipolar Primate retinal ganglion cells expressing melanopsin cells also made synapses en passant with the dendrites were first identified by using in situ hybridization with a of outer stratifying melanopsin cells (Grunert et al., probe derived from human melanopsin. Labeled somas 2011). In human retinas, there were extensive interac- were observed in both the inner nuclear layer (INL) and tions between dopaminergic processes and processes the ganglion cell layer (GCL) of the macaque retina. Given labeled with antibodies to melanopsin. These were all the large size and sparse distribution of the somas, the interpreted as synapses from the dopaminergic amacrine authors proposed that the retinal ganglion cells projected cells onto melanopsin ganglion cell dendrites (Vugler to the suprachiasmatic nucleus of the hypothalamus et al., 2007). However, a recent study of mouse and mac- (Provencio et al., 2000). The morphology of the melanop- aque retina suggests that melanopsin ganglion cells sin ganglion cells in humans was first described, and pitu- transmit information in the opposite direction. The axons itary adenylate cyclase-activating polypeptide (PACAP), of a subset of melanopsin cells had collaterals that termi- the neuropeptide known to be present in retinal ganglion nated in both the inner and the outer IPL, suggesting that cells projecting to the hypothalamus, was colocalized in melanopsin cells are presynaptic at their terminals (Joo their somas (Hannibal et al., 2004). A retrograde labeling et al., 2013). study in macaques indicated that the melanopsin cells Several questions about melanopsin cells in primates also project to the LGN as well as to the pretectum remain unresolved, however. The synapses from ama- (Dacey et al., 2005). This finding in macaque was con- crine cells and bipolar cells onto melanopsin cells in firmed and extended to include other image- and primates have been observed via light microscopy, but nonimage-forming visual targets such as the suprachias- their ultrastructure has not been described. In other matic nucleus (SCN) and the superior colliculus (SC) in a mammals, there appears to be a third type of melanop- study of PACAP-immunoreactive retinal projections (Han- sin ganglion cell whose dendrites branch in two differ- nibal et al., 2014). In both humans and macaques, there ent strata of the IPL (Schmidt and Kofuji, 2011), but it were two types of melanopsin ganglion cells, those with is uncertain whether this type exists in primates. In dendrites primarily in the outermost stratum of the inner mouse retina, melanopsin cells play a role in pattern plexiform layer (IPL) and those with dendrites primarily in vision (Ecker et al., 2010), and the same may be true the innermost stratum (Hannibal et al., 2004, 2014; in primates. Therefore, it is important to know the spa- Dacey et al., 2005). In macaque, both types of melanop- tial distribution of their melanopsin cells. It is not clear sin cells depolarized and fired action potentials in how many melanopsin cells of each type cover a given response to increments of light stimuli under photopic retinal area, and the previous estimates of the spatial conditions (Dacey et al., 2005). The inner stratifying type density of the melanopsin ganglion cells in primate reti- also had ON responses like those to dim stimuli, indicat- nas vary widely (Hannibal et al., 2004; La Morgia et al., ing that they received input from rods. At higher light 2010). These questions are addressed in the experi- intensities, the polarity of their responses depended on ments described here. the wavelength of the stimulus. The inner stratifying mel- anopsin cells were inhibited by short-wavelength stimuli
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