Vesicular Glutamate Transporter 1 Is Required for Photoreceptor Synaptic Signaling But Not For Intrinsic Visual Functions

Johnson, John L.; Fremeau, Robert T.; Duncan, Jacque L.; Renterı́a, René C.; Yang, Hongbo; Hua, Zhaolin; Liu, Xiaorong; LaVail, Matthew M.; Edwards, Robert H.; Copenhagen, David R.

doi:10.1523/jneurosci.0815-07.2007

Cited by 48 publications

(51 citation statements)

References 43 publications

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“…Figure 3B shows the mixture of NBQX, AP5, AP4, and DHβE (middle trace) (11,30) effectively blocks the short latency photoreceptordriven responses in RGCs recorded from a P16 WT mouse (top trace). This same mixture of synaptic blockers failed to block the light-driven ipRGC responses in a P8 WT mouse (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Physiologically, in mouse retina, melanopsin-expressing ipRGCs can be activated by light as early as the day of birth (9,10). Concomitantly, by postnatal day 1 (P1), ipRGCs express vesicular glutamate transporter type 2, necessary for the synaptic release of glutamate from ipRGCs (11), and project their axons to the suprachiasmatic nucleus (SCN) of the hypothalamus (12). Furthermore, the retina-SCN tract in rats can be activated by light immediately after birth (9,10,13).…”

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confidence: 99%

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Melanopsin-dependent light avoidance in neonatal mice

Johnson¹,

Wu²,

Donovan³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

126

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Melanopsin-expressing, intrinsically photosensitive retinal ganglion cells (ipRGCs) form a light-sensitive system separate from rods and cones. Direct light stimulation of ipRGCs can regulate many nonimageforming visual functions such as photoentrainment of circadian rhythms and pupil responses, and can intensify migraine headache in adults. In mice, ipRGCs are light responsive as early as the day of birth. In contrast, their eyelids do not open until 12-13 d after birth (P12-13), and light signaling from rods and cones does not begin until approximately P10. No physiological or behavioral function is established for ipRGCs in neonates before the onset of rod and cone signaling. Here we report that mouse pups as young as P6 will completely turn away from a light. Light-induced responses of ipRGCs could be readily recorded in retinas of pups younger than P9, and we found no evidence for rod-and cone-mediated visual signaling to the RGCs of these younger mice. These results confirm that negative phototaxis is evident before the onset of rod-and cone-mediated visual signaling, and well before the onset of image-forming vision. Negative phototaxis was absent in mice lacking melanopsin. We conclude that light activation of melanopsin ipRGCs is necessary and sufficient for negative phototaxis. These results strongly suggest that light activation of ipRGCs may regulate physiological functions such as sleep/wake cycles in preterm and neonatal infants.

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Melanopsin-dependent light avoidance in neonatal mice

Johnson¹,

Wu²,

Donovan³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

126

View full text Add to dashboard Cite

show abstract

“…AG208) eliminates immunostaining (manufacturer's worksheet). No immunostaining was observed when this antibody was used on VGLUT1 knockout mouse retina (Johnson et al, 2007).…”

Section: Antibody Characterizationmentioning

confidence: 96%

Synaptotagmins I and II in the developing rat auditory brainstem: Synaptotagmin I is transiently expressed in glutamate‐releasing immature inhibitory terminals

Cooper

Gillespie

2011

J of Comparative Neurology

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The lateral superior olive (LSO), a nucleus in the auditory brainstem, computes interaural intensity differences for sound localization by comparing converging excitatory and inhibitory inputs that carry tonotopically matched information from the two ears. Tonotopic refinement in the inhibitory projection pathway from the medial nucleus of the trapezoid body (MNTB) is known to be established during the first postnatal week in rats. During this period, immature MNTB terminals in the LSO contain vesicular transporters for both inhibitory and excitatory amino acids and release glutamate. The primary Ca(2+) sensors for vesicular release in the CNS are understood to be synaptotagmins, and in adult auditory brainstem synaptotagmin 2 is the predominant synaptotagmin. We asked here whether a different Ca(2+) sensor might be expressed in the immature auditory brainstem. We have found that synaptotagmin 1 is indeed expressed transiently in the immature auditory brainstem, most highly in those areas that receive glutamate-releasing immature inhibitory inputs from the MNTB, and that during the first postnatal week synaptotagmin 1 co-localizes with the vesicular glutamate transporter VGLUT3, a marker of glutamate-releasing immature inhibitory terminals from the MNTB. We suggest that immature MNTB terminals may contain two populations of synaptic vesicles, one expressing the vesicular inhibitory amino acid transporter together with synaptotagmin 2 and another expressing VGLUT3 together with synaptotagmin 1. Because Ca(2+) sensing is an important determinant of release properties for the presynaptic terminal, differential expression of the synaptotagmins might allow the differential release of excitatory and inhibitory neurotransmitters in response to differing patterns of neural activity.

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“…RGCs sending axon collaterals into the IPL have been described in cat (Dacey 1985), monkey (Usai et al 1991) and human retina (Peterson and Dacey 1998); in human retina ~2% the RGCs examined had intraretinal axon collaterals that terminated in the outer half of the IPL and arose from RGCs with sparsely branched monostratified dendritic trees that aborized in the ON sublayer of the IPL (Peterson and Dacey 1998). In the cat retina, a small number of varicose processes in the IPL stain for one of the isoforms of the vesicular glutamate transporter (VGLUT2) and it was suggested that these may represent RGC axon collaterals (Fyk-Kolodziej et al 2004); ipRGCs use glutamate as a neurotransmitter and express VGLUT2 (Johnson et al 2007;Engelund et al 2010). A preliminary report indicates that indeed some ipRGCs may send axon collaterals into the IPL (Joo et al 2011).…”

Section: Iprgcs Provide Excitatory Drive To Dopaminergic Amacrine Cellsmentioning

confidence: 99%

Intrinsically Photosensitive Retinal Ganglion Cells

Pickard

Sollars

2011

Reviews of Physiology, Biochemistry and Pharmacology 162

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Intrinsically photosensitive retinal ganglion cells (ipRGCs) respond to light in the absence of all rod and cone photoreceptor input. The existence of these ganglion cell photoreceptors, although predicted from observations scattered over many decades, was not established until it was shown that a novel photopigment, melanopsin, was expressed in retinal ganglion cells of rodents and primates. Phototransduction in mammalian ipRGCs more closely resembles that of invertebrate than vertebrate photoreceptors and appears to be mediated by transient receptor potential channels. In the retina, ipRGCs provide excitatory drive to dopaminergic amacrine cells and ipRGCs are coupled to GABAergic amacrine cells via gap junctions. Several subtypes of ipRGC have been identified in rodents based on their morphology, physiology and expression of molecular markers. ipRGCs convey irradiance information centrally via the optic nerve to influence several functions including photoentrainment of the biological clock located in the hypothalamus, the pupillary light reflex, sleep and perhaps some aspects of vision. In addition, ipRGCs may also contribute irradiance signals that interface directly with the autonomic nervous system to regulate rhythmic gene activity in major organs of the body. Here we review the early work that provided the motivation for searching for a new mammalian photoreceptor, the ground-breaking discoveries, current progress that continues to reveal the unusual properties of these neuron photoreceptors, and directions for future investigation.Keywords: Melanopsin, Circadian rhythms, Suprachiasmatic nucleus, Retina digitalcommons.unl.edu P i c k a r d & S o l l a r S i n R e v P h y s i o l B i o c h e m P h a R m a c o l1 6 2 ( 2 0 1 2 ) Early Hints of a Third Photoreceptor in the Mammalian RetinaThe perception of shapes, color and objects moving in the world begins in the outer retina where light is absorbed by photopigments that are integral membrane apoproteins (opsins) covalently linked to a retinaldehyde chromophore in the rod and cone photoreceptors. The capturing of photons by rod and cone photoreceptors initiates a signaling cascade in which photon capture is converted into an electrical signal. The simplest common pathway these signals take from the eye to the brain is from the photoreceptors to bipolar cells to ganglion cells. Retinal ganglion cells (RGCs) convey the signals centrally as action potentials, transmitted via their axons in the optic nerve, to higher brain regions for integration and the further processing required for conscious visual perception (Fig. 1). Among non-mammalian vertebrates, photoreceptors are also found in locations outside the retina, including the pineal gland and in the brain itself. These extra-ocular photoreceptors mediate tasks not associated directly with visual perception (non-image forming functions such as hormone regulation). However, since the pioneering descriptions of the vertebrate retina by Santiago Ramón y Cajal in the late 1800s, it was believed that t...

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Vesicular Glutamate Transporter 1 Is Required for Photoreceptor Synaptic Signaling But Not For Intrinsic Visual Functions

Cited by 48 publications

References 43 publications

Melanopsin-dependent light avoidance in neonatal mice

Melanopsin-dependent light avoidance in neonatal mice

Synaptotagmins I and II in the developing rat auditory brainstem: Synaptotagmin I is transiently expressed in glutamate‐releasing immature inhibitory terminals

Intrinsically Photosensitive Retinal Ganglion Cells

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