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The Journal of Neuroscience, July 4, 2007, 27(27):7245-7255; doi:10.1523/JNEUROSCI.0815-07.2007

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

Juliette Johnson,^1,2,5 Robert T. Fremeau, Jr,^2,4,5 Jacque L. Duncan,¹ René C. Rentería,^1,2,5 Haidong Yang,¹ Zhaolin Hua,^2,4,5 Xiaorong Liu,^1,2,5 Matthew M. LaVail,^1,3 Robert H. Edwards,^2,4,5 and David R. Copenhagen^1,2,5

Departments of ¹Ophthalmology, ²Physiology, ³Anatomy, and ⁴Neurology, and ⁵Program in Neurosciences, University of California School of Medicine, San Francisco, California 94143

Correspondence should be addressed to Dr. Juliette Johnson, Department of Ophthalmology, University of California, San Francisco, School of Medicine, 10 Kirkham Street, Room K-140, San Francisco, CA 94143-0730. Email: johnsonj{at}vision.ucsf.edu

Glutamatergic neurotransmission requires vesicular glutamate transporters (VGLUTs) to sequester glutamate into synaptic vesicles. Generally, VGLUT1 and VGLUT2 isoforms show complementary expression in the CNS and retina. However, little is known about whether isoform-specific expression serves distinct pathways and physiological functions. Here, by examining visual functions in VGLUT1-null mice, we demonstrate that visual signaling from photoreceptors to retinal output neurons requires VGLUT1. However, photoentrainment and pupillary light responses are preserved. We provide evidence that melanopsin-containing, intrinsically photosensitive retinal ganglion cells (RGCs), signaling via VGLUT2 pathways, support these non-image-forming functions. We conclude that VGLUT1 is essential for transmitting visual signals from photoreceptors to second- and third-order neurons, but VGLUT1 is not necessary for intrinsic visual functions. Furthermore, melanopsin and VGLUT2 expression in a subset of RGCs immediately after birth strongly supports the idea that intrinsic vision can function well before rod- and cone-mediated signaling has matured.

Key words: ERG; VEP; immunohistochemistry; photoentrainment; pupillary light response; multielectrode array

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Received Feb. 22, 2007; revised May 21, 2007; accepted May 23, 2007.

Correspondence should be addressed to Dr. Juliette Johnson, Department of Ophthalmology, University of California, San Francisco, School of Medicine, 10 Kirkham Street, Room K-140, San Francisco, CA 94143-0730. Email: johnsonj{at}vision.ucsf.edu

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