Divergent outer retinal circuits drive image and non-image visual behaviors

Beier, Corinne; Bocchero, Ulisse; Levy, Lior; Zhang, Zhijing; Jin, Nange; Massey, Stephen C.; Ribelayga, Christophe; Martemyanov, Kirill A.; Hattar, Samer; Pahlberg, Johan

doi:10.1016/j.celrep.2022.111003

Cited by 15 publications

(18 citation statements)

References 77 publications

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“…Using novel mouse models that lack rod/cone coupling, 84 we were able to demonstrate the profound impact of rod/cone coupling plasticity on the light responses of cones, 84 and subsequently second‐order 86 and third‐order neurons 87 . Remarkably, eliminating rod/cone coupling decreases the amplitude of pupillary light reflex under dim light, thereby revealing its functional importance in the performance of a visual function 88 . Thus, the suppression of dopamine release at night and subsequent increase in rod/cone coupling observed in many vertebrate species, including fish and mouse, suggest a conserved function for melatonin in enhancing transmission of rod signals to second‐ and third‐order neurons and thereby promoting dark adaptation and increasing the sensitivity to light of visual circuits.…”

Section: Melatonin Synthesismentioning

confidence: 93%

“…87 Remarkably, eliminating rod/cone coupling decreases the amplitude of pupillary light reflex under dim light, thereby revealing its functional importance in the performance of a visual function. 88 Thus, the suppression of dopamine release at night and subsequent increase in rod/cone coupling observed in many vertebrate species, including fish and mouse, suggest a conserved function for melatonin in enhancing transmission of rod signals to second-and third-order neurons and thereby promoting dark adaptation and increasing the sensitivity to light of visual circuits. This knowledge offers a conceptual framework to explore the functional reorganization of the photoreceptor network with the time of day and the role of melatonin in the retinal processing of visual information.…”

Section: The Role Of Melatonin In the Control Of Rod/cone Electrical ...mentioning

confidence: 99%

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Melatonin in the mammalian retina: Synthesis, mechanisms of action and neuroprotection

Felder‐Schmittbuhl,

Hicks,

Ribelayga

et al. 2024

Journal of Pineal Research

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Melatonin is an important player in the regulation of many physiological functions within the body and in the retina. Melatonin synthesis in the retina primarily occurs during the night and its levels are low during the day. Retinal melatonin is primarily synthesized by the photoreceptors, but whether the synthesis occurs in the rods and/or cones is still unclear. Melatonin exerts its influence by binding to G protein‐coupled receptors named melatonin receptor type 1 (MT1) and type 2 (MT2). MT1 and MT2 receptors activate a wide variety of signaling pathways and both receptors are present in the vertebrate photoreceptors where they may form MT1/MT2 heteromers (MT1/2h). Studies in rodents have shown that melatonin signaling plays an important role in the regulation of retinal dopamine levels, rod/cone coupling as well as the photopic and scotopic electroretinogram. In addition, melatonin may play an important role in protecting photoreceptors from oxidative stress and can protect photoreceptors from apoptosis. Critically, melatonin signaling is involved in the modulation of photoreceptor viability during aging and other studies have implicated melatonin in the pathogenesis of age‐related macular degeneration. Hence melatonin may represent a useful tool in the fight to protect photoreceptors—and other retinal cells—against degeneration due to aging or diseases.

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Section: Melatonin Synthesismentioning

confidence: 93%

Section: The Role Of Melatonin In the Control Of Rod/cone Electrical ...mentioning

confidence: 99%

Melatonin in the mammalian retina: Synthesis, mechanisms of action and neuroprotection

Felder‐Schmittbuhl,

Hicks,

Ribelayga

et al. 2024

Journal of Pineal Research

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“…Light responses from rod photoreceptors and rod bipolar cells were recorded from retinal slices as previously described ( Pahlberg et al, 2018 ; Beier et al, 2022 ). Briefly, slices were obtained from mice dark-adapted overnight and euthanized according to protocols and guidelines approved by the NIH.…”

Section: Methodsmentioning

confidence: 99%

Frmpd1 Facilitates Trafficking of G-Protein Transducin and Modulates Synaptic Function in Rod Photoreceptors of Mammalian Retina

Campla

Bocchero

Strickland

et al. 2022

eNeuro

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“…This organization has potential functional significance as axonal inputs, at least from the retina, innervate some regions of vLGN but not others. For example, neurons within the lateral-most external domain of vLGN (vLGNe), receive monosynaptic input from RGCs, whereas those in the medial, internal vLGN (vLGNi) do not appear to be retinorecipient ( Hammer et al, 2014 ; Sabbagh et al, 2021 ; Beier et al, 2022 ). Indeed, these cell type-specific circuits are likely to underlie differences in the emerging functions of vLGN, which include light-mediated effects on depressive behavior, innate escape responses to visual threats ( Huang et al, 2019 ; Fratzl et al, 2021 ; Huang et al, 2021 ; Salay and Huberman, 2021 ; Fratzl and Hofer, 2022 ), as well as oculomotor signaling and the photic regulation of circadian rhythms ( Magnin et al, 1974 ; Harrington, 1997 ; Livingston and Fedder, 2003 ).…”

Section: Introductionmentioning

confidence: 99%

“…Retinal axons innervating target neurons in vLGN differ significantly in structure and function from canonical retinogeniculate synapses in dLGN ( Hammer et al, 2014 ). Neurons in vLGN have diffusely organized receptive fields and receive input from both image-forming and non-image-forming RGCs ( Monavarfeshani et al, 2017 ; Ciftcioglu et al, 2020 ; Beier et al, 2022 ). However, they do exhibit some features associated with driver inputs, such as large ionotropic glutamatergic synaptic responses that exhibit depression following repetitive stimulation ( Petrof and Sherman, 2013 ; Hammer et al, 2014 ; Sabbagh et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Pattern of Driver-Like Input onto Neurons of the Mouse Ventral Lateral Geniculate Nucleus

Govindaiah

Fox

Guido

2023

eNeuro

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The ventral lateral geniculate nucleus (vLGN) is a retino-recipient region of thalamus that contributes to a number of complex visual behaviors. Retinal axons that target vLGN terminate exclusively in the external subdivision (vLGNe), which is also transcriptionally and cytoarchitectonically distinct from the internal subdivision (vLGNi). While recent studies shed light on the cell types and efferent projections of vLGNe and vLGNi, we have a crude understanding of the source and nature of the excitatory inputs driving postsynaptic activity in these regions. Here, we address this by conductingin vitrowhole cell recordings in acutely prepared thalamic slices and employing electrical and optical stimulation techniques to examine the postsynaptic excitatory activity evoked by the activation of retinal or cortical layer V input onto neurons in vLGNe and vLGNi. Activation of retinal afferents by electrical stimulation of optic tract or optical stimulation of retinal terminals resulted in robust driver-like excitatory activity in vLGNe. Optical activation of corticothalamic terminals from layer V resulted in similar driver-like activity in both vLGNe and vLGNi. Using a dual color optogenetic approach, we found that many vLGNe neurons received convergent input from these two sources. Both individual pathways displayed similar driver-like properties, with corticothalamic stimulation leading to a stronger form of synaptic depression than retinogeniculate stimulation. We found no evidence of convergence in vLGNi, with neurons only responding to corticothalamic stimulation. These data provide insight into the influence of excitatory inputs to vLGN and reveal that only neurons in vLGNe receive convergent input from both sources.SIGNIFICANCE STATEMENTThe ventral lateral geniculate nucleus is traditionally thought of as a thalamic visual recipient structure. However, recent studies reveal its divergent output to a variety of nonvisual subcortical structures helps control an array of light-mediated defensive and mood related behaviors. Despite this knowledge, we still lack an understanding of where and how inputs to this nucleus drive activity. Here we show that vLGN receives strong, driver-like excitatory input from two sources, the retina and cortical layer V. The external subdivision receives convergent input from both sources, whereas the internal division receives input only from layer V. Such an arrangement has important implications for understanding the functional organization of vLGN and its role in integrating vision with internal behavioral states.

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Divergent outer retinal circuits drive image and non-image visual behaviors

Cited by 15 publications

References 77 publications

Melatonin in the mammalian retina: Synthesis, mechanisms of action and neuroprotection

Melatonin in the mammalian retina: Synthesis, mechanisms of action and neuroprotection

Frmpd1 Facilitates Trafficking of G-Protein Transducin and Modulates Synaptic Function in Rod Photoreceptors of Mammalian Retina

Pattern of Driver-Like Input onto Neurons of the Mouse Ventral Lateral Geniculate Nucleus

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