Intrinsically photosensitive ganglion cells of the primate retina express distinct combinations of inhibitory neurotransmitter receptors

Neumann, Sonja; Haverkamp, Silke; Auferkorte, Olivia N.

doi:10.1016/j.neuroscience.2011.10.027

Cited by 18 publications

(17 citation statements)

References 39 publications

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“…Our double label immunohistochemistry shows that outer as well as inner melanopsin‐expressing cells in human retina have postsynaptic densities on their dendrites and thus are likely to receive synaptic input via bipolar cells. Consistently, there is evidence in non‐human primates from electrophysiological recordings demonstrating synaptic input at light levels below the range of a melanopsin‐dependent photoreceptive pathway (Dacey et al, ) as well as from light and electron microscopy showing bipolar and amacrine input (Grünert et al, ; Jusuf et al, ; Liao et al, ; Neumann, Haverkamp, & Auferkorte, ). Some of the bipolar input to melanopsin cells in macaque and marmoset retinas to both the outer as well as to the inner dendrites derives from DB6 bipolar cells (Grünert et al, ; Jusuf et al, ; Liao et al, ).…”

Section: Discussionmentioning

confidence: 71%

Melanopsin‐expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections

Nasir-Ahmad

Lee

Martin

et al. 2017

J of Comparative Neurology

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Melanopsin-expressing retinal ganglion cells are intrinsically photosensitive cells that are involved in non-image forming visual processes such as the pupillary light reflex and circadian entrainment but also contribute to visual perception. Here we used immunohistochemistry to study the morphology, density, distribution, and synaptic connectivity of melanopsin-expressing ganglion cells in four post mortem human donor retinas. Two types of melanopsin-expressing ganglion cells were distinguished based on their dendritic stratification near either the outer or the inner border of the inner plexiform layer. Outer stratifying cells make up on average 60% of the melanopsin-expressing cells. About half of the melanopsin-expressing cells (or 80% of the outer stratifying cells) have their soma displaced to the inner nuclear layer. Inner stratifying cells have their soma exclusively in the ganglion cell layer and include a small proportion of bistratified cells. The dendritic field diameter of melanopsin-expressing cells ranges from 250 (near the fovea) to 1,000 µm in peripheral retina. The dendritic trees of outer stratifying cells cover the retina independent of soma location. The dendritic fields of both outer and inner stratifying cells show a high degree of overlap with a coverage factor of approximately two. Melanopsin-expressing cells occur at an average peak density of between ∼20 and ∼40 cells/mm at about 2 mm eccentricity, the density drops to below ∼10 cells/mm at about 8 mm eccentricity. Both the outer and inner stratifying dendrites express postsynaptic density (PSD95) immunoreactive puncta suggesting that they receive synaptic input from bipolar cells.

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Section: Discussionmentioning

confidence: 71%

Melanopsin‐expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections

Nasir-Ahmad

Lee

Martin

et al. 2017

J of Comparative Neurology

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“…In one case, the dendrites were monostratified in the outermost stratum of the IPL, whereas the dendrites of the second type were located mainly in the innermost stratum. This anatomical description of primate melanopsin cells, which are similar to rodent M1 and M2 cells, was later confirmed (Dkhissi-Benyahya et al, 2006; La Morgia et al, 2010; Neumann et al, 2011) and the cells have been referred to accordingly (Neumann et al, 2011). …”

Section: Discussionmentioning

confidence: 79%

Loss of Melanopsin-Expressing Ganglion Cell Subtypes and Dendritic Degeneration in the Aging Human Retina

Esquiva

Lax

Pérez-Santonja

et al. 2017

Front. Aging Neurosci.

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In mammals, melanopsin-expressing retinal ganglion cells (mRGCs) are, among other things, involved in several non-image-forming visual functions, including light entrainment of circadian rhythms. Considering the profound impact of aging on visual function and ophthalmic diseases, here we evaluate changes in mRGCs throughout the life span in humans. In 24 post-mortem retinas from anonymous human donors aged 10–81 years, we assessed the distribution, number and morphology of mRGCs by immunostaining vertical retinal sections and whole-mount retinas with antibodies against melanopsin. Human retinas showed melanopsin immunoreactivity in the cell body, axon and dendrites of a subset of ganglion cells at all ages tested. Nearly half of the mRGCs (51%) were located within the ganglion cell layer (GCL), and stratified in the outer (M1, 12%) or inner (M2, 16%) margin of the inner plexiform layer (IPL) or in both plexuses (M3, 23%). M1 and M2 cells conformed fairly irregular mosaics, while M3 cell distribution was slightly more regular. The rest of the mRGCs were more regularly arranged in the inner nuclear layer (INL) and stratified in the outer margin of the IPL (M1d, 49%). The quantity of each cell type decrease after age 70, when the total number of mRGCs was 31% lower than in donors aged 30–50 years. Moreover, in retinas with an age greater than 50 years, mRGCs evidenced a decrease in the dendritic area that was both progressive and age-dependent, as well as fewer branch points and terminal neurite tips per cell and a smaller Sholl area. After 70 years of age, the distribution profile of the mRGCs was closer to a random pattern than was observed in younger retinas. We conclude that advanced age is associated with a loss in density and dendritic arborization of the mRGCs in human retinas, possibly accounting for the more frequent occurrence of circadian rhythm disorders in elderly persons.

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“…Both types have sparse dendrites and monostratify in either the ON or OFF sublamina. Thus, they resemble the M1 and M2 cells of rodents, and have been referred to as such (Neumann et al, 2011). However, these primate RGCs are not functionally equivalent to the M1 and M2 cells.…”

Section: Discussionmentioning

confidence: 99%

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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Intrinsically photosensitive ganglion cells of the primate retina express distinct combinations of inhibitory neurotransmitter receptors

Cited by 18 publications

References 39 publications

Melanopsin‐expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections

Melanopsin‐expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections

Loss of Melanopsin-Expressing Ganglion Cell Subtypes and Dendritic Degeneration in the Aging Human Retina

The rat retina has five types of ganglion-cell photoreceptors

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