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

Nasir-Ahmad, Subha; Lee, Sammy; Martin, Paul R.; Grünert, Ulrike

doi:10.1002/cne.24176

Cited by 78 publications

(95 citation statements)

References 50 publications

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“…This view is established for rodents and is likely to hold across species (e.g. Hannibal et al, 2017; Hannibal et al, 2014; Nasir-Ahmad et al, 2017). It is against this background of stereotyped features that we have found extreme, continuous, and flexible variation in the biophysical parameters of M1s.…”

Section: Discussionmentioning

confidence: 93%

Biophysical Variation within the M1 Type of Ganglion Cell Photoreceptor

Emanuel

Kapur

2017

Cell Reports

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Summary Intrinsically photosensitive retinal ganglion cells of the M1 type encode environmental irradiance for functions that include circadian and pupillary regulation. Their distinct role, morphology, and molecular markers indicate that they are stereotyped circuit elements—however, their physiological uniformity has not been investigated in a systematic fashion. We have profiled the biophysical parameters of mouse M1s and found that extreme variation is their hallmark. Most parameters span 1-3 log units, and the full range is evident in M1s that innervate brain regions serving divergent functions. Biophysical profiles differ among cells possessing similar morphology, and between neighboring M1s recorded simultaneously. Variation in each parameter is largely independent of that in others, allowing for flexible individualization. Accordingly, a common stimulus drives heterogeneous spike outputs across cells. By contrast, a population of directionally selective retinal ganglion cells appeared physiologically uniform under similar conditions. Thus, M1s lack biophysical constancy and send diverse signals downstream.

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Section: Discussionmentioning

confidence: 93%

Biophysical Variation within the M1 Type of Ganglion Cell Photoreceptor

Emanuel

Kapur

2017

Cell Reports

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“…M1 and M2 cells have dendrites limited to S1 and S5, respectively, and each appears to tile the retina. M1 cells are immunolabeled more strongly for melanopsin than M2 cells, suggesting a higher expression level of the protein (Liao et al, ; Nasir‐Ahmad et al, ). M3 cells have also been observed in primate (Nasir‐Ahmad et al, ), though as with rodents, these cells are rare and may arise just from morphological variability in another ipRGC type.…”

Section: Discussionmentioning

confidence: 99%

“…M1 cells are immunolabeled more strongly for melanopsin than M2 cells, suggesting a higher expression level of the protein (Liao et al, ; Nasir‐Ahmad et al, ). M3 cells have also been observed in primate (Nasir‐Ahmad et al, ), though as with rodents, these cells are rare and may arise just from morphological variability in another ipRGC type. Unlike mice, the diversity and organization of ipRGCs in primate is currently limited to immunolabeling, which may result in a failure to identify RGCs with weaker expression levels of melanopsin, such as M4 and M5 cells in rodent.…”

Section: Discussionmentioning

confidence: 99%

Distribution and diversity of intrinsically photosensitive retinal ganglion cells in tree shrew

Johnson

Westbrook

Shayesteh

et al. 2017

J of Comparative Neurology

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Intrinsically photosensitive retinal ganglion cells (ipRGCs) mediate the pupillary light reflex, circadian entrainment, and may contribute to luminance and color perception. The diversity of ipRGCs varies from rodents to primates, suggesting differences in their contributions to retinal output. To further understand the variability in their organization and diversity across species, we used immunohistochemical methods to examine ipRGCs in tree shrew (Tupaia belangeri). Tree shrews share membership in the same clade, or evolutionary branch, as rodents and primates. They are highly visual, diurnal animals with a cone-dominated retina and a geniculo-cortical organization resembling that of primates. We identified cells with morphological similarities to M1 and M2 cells described previously in rodents and primates. M1-like cells typically had somas in the ganglion cell layer, with 23% displaced to the inner nuclear layer (INL). However, unlike M1 cells, they had bistratified dendritic fields ramifying in S1 and S5 that collectively tiled space. M2-like cells had dendritic fields restricted to S5 that were smaller and more densely branching. A novel third type of melanopsin immunopositive cell was identified. These cells had somata exclusively in the INL and monostratified dendritic fields restricted to S1 that tiled space. Surprisingly, these cells immunolabeled for tyrosine hydroxylase, a key component in dopamine synthesis. These cells immunolabeled for an RGC marker, not amacrine cell markers, suggesting that they are dopaminergic ipRGCs. We found no evidence for M4 or M5 ipRGCs, described previously in rodents. These results identify some organizational features of the ipRGC system that are canonical versus species-specific.

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“…In light microscopic double labeling experiments, one type of retinal ganglion cell whose dendrites made contacts with the secretoneurin-IR dendrites was identified as the outer-stratifying melanopsin cell [17, 20]. Additional subtypes of human retinal ganglion cells containing melanopsin have been described recently [32], but they were not identified in this study.…”

Section: Discussionmentioning

confidence: 92%

“…Dendrites of intrinsically-photosensitve retinal ganglion cells containing the photopigment melanopsin are found in both S1 and S5 [17, 20]. Contacts with dendrites of secretoneurin-IR amacrine cells were observed in double immunolabeling experiments using antibody to melanopsin.…”

Section: Resultsmentioning

confidence: 99%

Wavy multistratified amacrine cells in the monkey retina contain immunoreactive secretoneurin

Bordt¹,

Long²,

Kouyama

et al. 2017

Peptides

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The goals of this study were to describe the morphology, neurotransmitter content and synaptic connections of neurons in primate retinas that contain the neuropeptide secretoneurin. Amacrine cells were labeled with antibodies to secretoneurin in macaque and baboon retinas. Their processes formed three distinct plexuses in the inner plexiform layer: one in the outermost stratum, one in the center and one in the innermost stratum. In light microscopic double immunolabeling experiments, GABA was colocalized with secretoneurin in these cells, but glycine transporter 1 and Substance P were not. ON bipolar cell axon terminals labeled with antibody to the cholecystokinin precursor, G6-gly, have ON responses to stimulation of short wavelength sensitive (S) cones. Axons of these bipolar cells made contacts with amacrine cell dendrites containing secretoneurin. Secretoneurin-IR amacrine cells also made contacts with retinal ganglion cell dendrites labeled with antibody to the photopigment melanopsin, which have OFF responses to stimulation of S cones. Using electron microscopic immunolabeling, 436 synapses from macaque retina were analyzed. Axons from bipolar cells were identified by their characteristic synaptic ribbons; their synaptic densities were asymmetric like those of excitatory synapses in the brain. Amacrine cells made and received conventional synapses with symmetric synaptic densities, like those of inhibitory synapses in the brain. Ganglion cell dendrites were identified by their absence of presynaptic specializations; they received inputs from both amacrine cells and bipolar cells. The majority of inputs to the secretoneurin-IR amacrine cells were from other amacrine cells, but they also received 21% of their input from bipolar cells. They directed most of their output, 54%, to amacrine cells, but there were many synapses onto bipolar cell axons and ganglion cell dendrites, as well. The synaptic connections were very similar in the three plexuses with one notable exception; output synapses to bipolar cells were significantly less common in the innermost one, where the S-ON bipolar cells terminate. Taken together, these findings suggest that the secretoneurin-IR amacrine cells in primates receive excitatory input from S-ON bipolar cells and, in turn, inhibit intrinsically photosensitive retinal ganglion cells.

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

Cited by 78 publications

References 50 publications

Biophysical Variation within the M1 Type of Ganglion Cell Photoreceptor

Biophysical Variation within the M1 Type of Ganglion Cell Photoreceptor

Distribution and diversity of intrinsically photosensitive retinal ganglion cells in tree shrew

Wavy multistratified amacrine cells in the monkey retina contain immunoreactive secretoneurin

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