Parallel Inhibition of Dopamine Amacrine Cells and Intrinsically Photosensitive Retinal Ganglion Cells in a Non-Image-Forming Visual Circuit of the Mouse Retina

Vuong, Helen E.; Hardi, Claudia N.; Barnes, Steven; Brecha, Nicholas C.

doi:10.1523/jneurosci.3382-15.2015

Cited by 37 publications

(37 citation statements)

References 67 publications

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“… 39 Although we believe that TCS OX229 enhances melanopsin-based DAC responses via blockade of OX 2 R, it is possible that TCS OX229-induced potentiation also occurs via blockade of OX 1 R. Further investigations are needed to clarify this issue. Regardless, our results clearly suggest that exogenous and endogenous orexins downregulate intraretinal retrograde signaling via activation of OX 1 R and possibly OX 2 R. In conjunction with a recent study showing that the neuropeptide somatostatin suppressed signal transmission between ipRGCs and DACs, 41 our results suggest that neuropeptides are likely to play an important role in modulating retrograde signaling in the retina.…”

Section: Discussionsupporting

confidence: 84%

Orexin-A Suppresses Signal Transmission to Dopaminergic Amacrine Cells From Outer and Inner Retinal Photoreceptors

Qiao

Zhou

Liu

et al. 2017

Invest. Ophthalmol. Vis. Sci.

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PurposeThe neuropeptides orexin-A and orexin-B are widely expressed in the vertebrate retina; however, their role in visual function is unclear. This study investigates whether and how orexins modulate signal transmission to dopaminergic amacrine cells (DACs) from both outer retinal photoreceptors (rods and cones) and inner retinal photoreceptors (melanopsin-expressing intrinsically photosensitive retinal ganglion cells [ipRGCs]).MethodsA whole-cell voltage-clamp technique was used to record light-induced responses from genetically labeled DACs in flat-mount mouse retinas. Rod and cone signaling to DACs was confirmed pharmacologically (in wild-type retinas), whereas retrograde melanopsin signaling to DACs was isolated either pharmacologically (in wild-type retinas) or by genetic deletion of rod and cone function (in transgenic mice).ResultsOrexin-A attenuated rod/cone-mediated light responses in the majority of DACs and inhibited all DACs that exhibited melanopsin-based light responses, suggesting that exogenous orexin suppresses signal transmission from rods, cones, and ipRGCs to DACs. In addition, orexin receptor 1 antagonist SB334867 and orexin receptor 2 antagonist TCS OX229 enhanced melanopsin-based DAC responses, indicating that endogenous orexins inhibit signal transmission from ipRGCs to DACs. We further found that orexin-A inhibits melanopsin-based DAC responses via orexin receptors on DACs, whereas orexin-A may modulate signal transmission from rods and cones to DACs through activation of orexin receptors on DACs and their upstream neurons.ConclusionsOur results suggest that orexins could influence visual function via the dopaminergic system in the mammalian retina.

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Section: Discussionsupporting

confidence: 84%

Orexin-A Suppresses Signal Transmission to Dopaminergic Amacrine Cells From Outer and Inner Retinal Photoreceptors

Qiao

Zhou

Liu

et al. 2017

Invest. Ophthalmol. Vis. Sci.

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“…The synthesis and release of dopamine are light‐driven as well as circadian regulated in birds and amphibians, but in mammalian retinas that are melatonin‐deficient, their retinal dopamine content only displays a diurnal rhythm (Iuvone et al., ; Nir, Haque, & Iuvone, 2000a, 2000b; Valenciano, Alonso‐Gomez, & Iuvone, ; Zhang, Silveyra, Jin, & Ribelayga, ). While previous studies showed that light stimulated DA amacrine cells by activating rods, cones, and the melanopsin‐expressing intrinsically photosensitive retina ganglion cells (Newkirk, Hoon, Wong, & Detwiler, ; Vuong, Hardi, Barnes, & Brecha, ; Zhang, Zhou, & McMahon, ; Zhang et al., ), a more comprehensive examination shows that it is the cone photoreceptors that drive the light signals through multiple neural circuits, including both ON and OFF bipolar cells, as well as a cone‐driven retrograde signaling pathway from ipRGCs, to modulate the dopamine release from DA amacrine cells (Qiao, Zhang, Ribelayga, Zhong, & Zhang, ).…”

Section: Circadian Integration In the Retinamentioning

confidence: 99%

Circadian regulation in the retina: From molecules to network

2018

Eur J of Neuroscience

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The mammalian retina is the most unique tissue among those that display robust circadian/diurnal oscillations. The retina is not only a light sensing tissue that relays light information to the brain, it has its own circadian “system” independent from any influence from other circadian oscillators. While all retinal cells and retinal pigment epithelium (RPE) possess circadian oscillators, these oscillators integrate by means of neural synapses, electrical coupling (gap junctions), and released neurochemicals (such as dopamine, melatonin, adenosine, and ATP), so the whole retina functions as an integrated circadian system. Dysregulation of retinal clocks not only causes retinal or ocular diseases, it also impacts the circadian rhythm of the whole body, as the light information transmitted from the retina entrains the brain clock that governs the body circadian rhythms. In this review, how circadian oscillations in various retinal cells are integrated, and how retinal diseases affect daily rhythms.

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“…If there was global inhibition, it could serve as a gain control mechanism that enhances the contrast between neuromasts that are more strongly stimulated and the ones that are less stimulated. Gain control by dopaminergic neurons is also known for dopaminergic groups in other sensory systems such as amacrine dopaminergic neurons in the retina [38] and olfactory bulb dopaminergic neurons [39]. Nevertheless, modulation of the motor circuits by the mechanosensory posterior tubercular dopaminergic system is also plausible, since farprojecting dopaminergic neurons also innervate hindbrain reticulospinal neurons and spinal cord motoneurons.…”

Section: A11-type Dopaminergic Activity Potentially Regulates the Senmentioning

confidence: 99%

The Descending Diencephalic Dopamine System Is Tuned to Sensory Stimuli

2017

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The vertebrate diencephalic A11 system provides the sole dopaminergic innervation of hindbrain and spinal cord and has been implicated in modulation of locomotion and sensory processes. However, the exact contributions of sensory stimuli and motor behavior to A11 dopaminergic activity remain unclear. We recorded cellular calcium activity in four anatomically distinct posterior tubercular A11-type dopaminergic subgroups and two adjacent hypothalamic dopaminergic groups in GCaMP7a-transgenic, semi-restrained zebrafish larvae. Our analyses reveal the contributions of different sensory modalities and motor states to dopaminergic activity. Each posterior tubercular and hypothalamic subgroup showed distinct activity patterns, while activity was synchronous within individual subgroups. Caudal and dorsomedial hypothalamic dopaminergic neurons are activated following vigorous tail movements and stay active for about 10 s, revealing predominantly post-motor activity. In contrast, posterior tubercular dopaminergic neurons are predominantly sensory driven, with subgroups differentially responding to different tactile or visual sensory modalities. In the anterior subgroups, neuronal response magnitudes are tuned to tactile stimulus intensities, revealing features similar to sensory systems. We identify the lateral line system as source for this tactile tuning. In contrast, the posterior subgroup is responsive to distinct moving visual stimuli. Specifically, translational forward stimuli, which may indicate insufficient rheotaxis and drift, induce dopaminergic activity, but backward or rotational stimuli not. The activation of posterior tubercular dopaminergic neurons by sensory stimuli, and their projections onto peripheral mechanosensory systems, suggests a participation of A11-type neurons in the feedback regulation of sensory systems. Together with the adjacent hypothalamic neurons, they may serve to set basic behavioral states.

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Parallel Inhibition of Dopamine Amacrine Cells and Intrinsically Photosensitive Retinal Ganglion Cells in a Non-Image-Forming Visual Circuit of the Mouse Retina

Cited by 37 publications

References 67 publications

Orexin-A Suppresses Signal Transmission to Dopaminergic Amacrine Cells From Outer and Inner Retinal Photoreceptors

Orexin-A Suppresses Signal Transmission to Dopaminergic Amacrine Cells From Outer and Inner Retinal Photoreceptors

Circadian regulation in the retina: From molecules to network

The Descending Diencephalic Dopamine System Is Tuned to Sensory Stimuli

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