Glutamatergic neurotransmission from melanopsin retinal ganglion cells is required for neonatal photoaversion but not adult pupillary light reflex

• Published in: PloS one 2013-12, Vol.8 (12), p.e83974-e83974
• Main Authors: Delwig, Anton, Majumdar, Sriparna, Ahern, Kelly, LaVail, Matthew M, Edwards, Robert, Hnasko, Thomas S, Copenhagen, David R
• Format: Article
• Language: English
• Subjects: Anatomy & physiology; Animals; Animals, Newborn; Aversion; Behavior, Animal; Biology; Brain; Clonal deletion; Female; Forming; Ganglion cysts; Glutamate; Glutamatergic transmission; Glutamic acid transporter; Immunoenzyme Techniques; Integrases - metabolism; Laboratory animals; Light; Light Signal Transduction; Male; Melanopsin; Mice; Mice, Knockout; Neonates; Neurons; Neurotransmission; Neurotransmitter Agents - metabolism; Neurotransmitters; Newborn babies; Newborn infants; Photic Stimulation; Photoreceptors; Phototaxis; Physiology; Pituitary adenylate cyclase-activating polypeptide; Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism; Polypeptides; Reflex, Pupillary - physiology; Reflex, Pupillary - radiation effects; Retina; Retinal ganglion cells; Retinal Ganglion Cells - metabolism; Retinal Ganglion Cells - radiation effects; Rod Opsins - physiology; Rodents; Signaling; Studies; Synaptic Transmission - physiology; Vesicular Glutamate Transport Protein 2 - physiology; Vision Disorders; Vision, Ocular - physiology; Vision, Ocular - radiation effects; Visual signals
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0083974

Melanopsin-expressing retinal ganglion cells (mRGCs) in the eye play an important role in many light-activated non-image-forming functions including neonatal photoaversion and the adult pupillary light reflex (PLR). MRGCs rely on glutamate and possibly PACAP (pituitary adenylate cyclase-activating polypeptide) to relay visual signals to the brain. However, the role of these neurotransmitters for individual non-image-forming responses remains poorly understood. To clarify the role of glutamatergic signaling from mRGCs in neonatal aversion to light and in adult PLR, we conditionally deleted vesicular glutamate transporter (VGLUT2) selectively from mRGCs in mice. We found that deletion of VGLUT2 in mRGCs abolished negative phototaxis and light-induced distress vocalizations in neonatal mice, underscoring a necessary role for glutamatergic signaling. In adult mice, loss of VGLUT2 in mRGCs resulted in a slow and an incomplete PLR. We conclude that glutamatergic neurotransmission from mRGCs is required for neonatal photoaversion but is complemented by another non-glutamatergic signaling mechanism for the pupillary light reflex in adult mice. We speculate that this complementary signaling might be due to PACAP neurotransmission from mRGCs.