Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina

Müller, Luis Pérez de Sevilla; H., Michael Tri; Yau, King Wai; He, Shunping; Baldridge, William H.

doi:10.1002/cne.22490

Cited by 79 publications

(73 citation statements)

References 61 publications

(123 reference statements)

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“…Not only do they have identical stratification patterns, but Sholl analyses of dendritic distribution are also in close agreement (Estevez et al, 2012; Hu et al, 2013; Muller et al, 2010; Schmidt and Kofuji, 2010, 2011). Comparison with three previous morphological characterizations of mouse M1 – M4 cells (Berson et al, 2010; Estevez et al, 2012; Schmidt and Kofuji, 2011) reveals additional similarities in soma size, total dendritic length, total branch points, and the number of primary dendrites.…”

Section: Discussionmentioning

confidence: 79%

The rat retina has five types of ganglion-cell photoreceptors

Reifler

Chervenak

Dolikian

et al. 2015

Experimental Eye Research

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Intrinsically photosensitive retinal ganglion cells (ipRGCs) are inner retinal photoreceptors that mediate non-image-forming visual functions, e.g. pupillary constriction, regulation of pineal melatonin release, and circadian photoentrainment. Five types of ipRGCs were recently discovered in mouse, but whether they exist in other mammals remained unknown. We report that the rat also has five types of ipRGCs, whose morphologies match those of mouse ipRGCs; this is the first demonstration of all five cell types in a non-mouse species. Through immunostaining and λmax measurements, we showed that melanopsin is likely the photopigment of all rat ipRGCs. The various cell types exhibited diverse spontaneous spike rates, with the M1 type spiking the least and M4 spiking the most, just like we had observed for their mouse counterparts. Also similar to mouse, all ipRGCs in rat generated not only sluggish intrinsic photoresponses but also fast, synaptically driven ones. However, we noticed two significant differences between these species. First, whereas we learned previously that all mouse ipRGCs had equally sustained synaptic light responses, rat M1 cells’ synaptic photoresponses were far more transient than those of M2–M5. Since M1 cells provide all input to the circadian clock, this rat-versus-mouse discrepancy could explain the difference in photoentrainment threshold between mouse and other species. Second, rat ipRGCs’ melanopsin-based spiking photoresponses could be classified into three varieties, but only two were discerned for mouse ipRGCs. This correlation of spiking photoresponses with cell types will help researchers classify ipRGCs in multielectrode-array (MEA) spike recordings.

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Section: Discussionmentioning

confidence: 79%

The rat retina has five types of ganglion-cell photoreceptors

Reifler

Chervenak

Dolikian

et al. 2015

Experimental Eye Research

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“…There are a number of examples of ipRGCs contacting other retinal neurons, both chemically and electrically. 6,20–24 However, to date this has been restricted to contacts with inner retinal neurons suggesting that such direct contacts are not sufficient to produce the range of effects we observe. An alternative explanation for our observed effects is a more global impact on the neuromodulatory environment of the retina, such as changes in inhibitory neuromodulators, signals of light adaptation, or even changes in the retinal pH, that could extend up to the photoreceptor level.…”

Section: Discussionmentioning

confidence: 86%

Chemogenetic Activation of ipRGCs Drives Changes in Dark-Adapted (Scotopic) Electroretinogram

Milosavljevic

Allen

Cehajic-Kapetanovic

et al. 2016

Invest. Ophthalmol. Vis. Sci.

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PurposeThe purpose of this study was to investigate the impact of activating melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) on dark-adapted (scotopic) electroretinograms (ERG).MethodsWe used mice (Opn4Cre/+) expressing cre recombinase in melanopsin-expressing cells for a targeted gene delivery of a chemogenetic Gq-coupled receptor, hM3Dq, to ipRGCs. Intraperitoneal injection of clozapine N-oxide (CNO) at 5 mg/kg was used for acute activation of hM3Dq and thus excitation of ipRGCs in darkness. Dark-adapted flash ERGs were recorded across a 9-fold range of irradiances from hM3Dq Opn4Cre/+ and control Opn4Cre/+ mice before and after intraperitoneal injection of CNO. A- and b-wave amplitudes and implicit times and oscillatory potentials (OPs) were analyzed. Paired-flash stimuli were used to isolate cone-driven responses.ResultsClozapine N-oxide application suppressed a- and b-wave amplitudes of the dark-adapted ERG across the flash intensity range in hM3Dq Opn4Cre/+ mice compared to control mice. Examination of the normalized irradiance-response functions revealed a shift in b-wave but not a-wave sensitivity. No changes in a- and b-wave implicit times were detected. Total OP amplitudes were also reduced in hM3Dq Opn4Cre/+ mice compared to controls following CNO administration. The paired-flash method revealed reduction in both the first (rods and cones) and second (cones only) flash response.ConclusionsAcute and selective activation of ipRGCs modulates the amplitude of both a- and b-waves of the scotopic ERG, indicating that the influence of this ganglion cell class on the retinal physiology extends to the photoreceptors as well as their downstream pathways.

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“…Intracellular injections were performed as described previously (Pérez de Sevilla Müller et al, 2007, Müller et al, 2010a, Müller et al, 2010b). tdTomato-expressing cells were visualized with a Zeiss 40X water-immersion objective.…”

Section: Methodsmentioning

confidence: 99%

Heterogeneous transgene expression in the retinas of the TH-RFP, TH-Cre, TH-BAC-Cre and DAT-Cre mouse lines

Vuong

Müller

Hardi³

et al. 2015

Neuroscience

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Transgenic mouse lines are essential tools for understanding the connectivity, physiology and function of neuronal circuits, including those in the retina. This report compares transgene expression in the retina of a tyrosine hydroxylase (TH)-red fluorescent protein (RFP) line with three catecholamine-related Cre recombinase lines [TH-bacterial artificial chromosome (BAC)-, TH-, and dopamine transporter (DAT)-Cre] that were crossed with a ROSA26-tdTomato reporter line. Retinas were evaluated and immunostained with commonly used antibodies including those directed to TH, GABA and glycine to characterize the RFP or tdTomato fluorescent-labeled amacrine cells, and an antibody directed to RNA-binding protein with multiple splicing to identify ganglion cells. In TH-RFP retinas, types 1 and 2 dopamine (DA) amacrine cells were identified by their characteristic cellular morphology and type 1 DA cells by their expression of TH immunoreactivity. In the TH-BAC-, TH-, and DAT-tdTomato retinas, less than 1%, ~6%, and 0%, respectively, of the fluorescent cells were the expected type 1 DA amacrine cells. Instead, in the TH-BAC-tdTomato retinas, fluorescently labeled AII amacrine cells were predominant, with some medium somal diameter ganglion cells. In TH-tdTomato retinas, fluorescence was in multiple neurochemical amacrine cell types, including four types of polyaxonal amacrine cells. In DAT-tdTomato retinas, fluorescence was in GABA immunoreactive amacrine cells, including two types of bistratified and two types of monostratified amacrine cells. Although each of the Cre lines were generated with the intent to specifically label DA cells, our findings show a cellular diversity in Cre expression in the adult retina and indicate the importance of careful characterization of transgene labeling patterns. These mouse lines with their distinctive cellular labeling patterns will be useful tools for future studies of retinal function and visual processing.

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Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina

Cited by 79 publications

References 61 publications

The rat retina has five types of ganglion-cell photoreceptors

The rat retina has five types of ganglion-cell photoreceptors

Chemogenetic Activation of ipRGCs Drives Changes in Dark-Adapted (Scotopic) Electroretinogram

Heterogeneous transgene expression in the retinas of the TH-RFP, TH-Cre, TH-BAC-Cre and DAT-Cre mouse lines

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