Seasonal and post-trauma remodeling in cone-dominant ground squirrel retina. (September 2016)

• Record Type: Journal Article
• Authors: Merriman, Dana K.; Sajdak, Benjamin S.; Li, Wei; Jones, Bryan W.
• Is Part Of: Experimental eye research. Volume 150(2016:Sep.)
• Page Start: 90
• Page End: 105
• Publication Date: 2016-09
• Subjects: Cone photoreceptor -- Microglia -- Müller cell -- Reactive gliosis -- Retinal detachment -- Retinal pigment epithelium -- Synaptic plasticity; AMD age-related macular degeneration -- AOSLO adaptive optics scanning light ophthalmoscopy -- CMP computational molecular phenotyping -- CNS central nervous system -- CRALBP cellular retinaldehyde binding protein -- CRMP-2 collapsin response mediator protein 2 -- CtBP2 C-terminal binding protein 2 -- DPYSL2 dihydropyrimidinase-like 2 -- EAAT1 excitatory amino acid transporter 1 -- ERG electroretinogram -- GFAP glial fibrillary acidic protein -- GS ground squirrel -- IBA interbout arousal -- IPL inner plexiform layer -- OCT optical coherence tomography -- ONL outer nuclear layer -- OLM outer limiting membrane -- OPL outer plexiform layer -- RBM3 RNA binding motif protein 3 -- RD retinal detachment -- RP retinitis pigmentosa -- RPE retinal pigment epithelium -- SCN suprachiasmatic nucleus -- SRS subretinal space -- TEM transmission electron microscopy -- 13LGS thirteen-lined ground squirrel; Ophthalmology -- Periodicals; Eye -- Periodicals; Œil -- Périodiques; Ophthalmology; Periodicals; Electronic journals; 612.8405
• DOI: 10.1016/j.exer.2016.01.011
• Languages: English
• ISSNs: 0014-4835

Abstract

Abstract: With a photoreceptor mosaic containing ∼85% cones, the ground squirrel is one of the richest known mammalian sources of these important retinal cells. It also has a visual ecology much like the human's. While the ground squirrel retina is understandably prominent in the cone biochemistry, physiology, and circuitry literature, far less is known about the remodeling potential of its retinal pigment epithelium, neurons, macroglia, or microglia. This review aims to summarize the data from ground squirrel retina to this point in time, and to relate them to data from other brain areas where appropriate. We begin with a survey of the ground squirrel visual system, making comparisons with traditional rodent models and with human. Because this animal's status as a hibernator often goes unnoticed in the vision literature, we then present a brief primer on hibernation biology. Next we review what is known about ground squirrel retinal remodeling concurrent with deep torpor and with rapid recovery upon re-warming. Notable here is rapidly-reversible, temperature-dependent structural plasticity of cone ribbon synapses, as well as pre- and post-synaptic plasticity throughout diverse brain regions. It is not yet clear if retinal cell types other than cones engage in torpor-associated synaptic remodeling. We end with the small but intriguing literature on the ground squirrel retina's remodeling responses to insult by retinal detachment. Notable for widespread loss of (cone) photoreceptors, there is surprisingly little remodeling of the RPE or Müller cells. Microglial activation appears minimal, and remodeling of surviving second- and third-order neurons seems absent, but both require further study. In contrast, traumatic brain injury in the ground squirrel elicits typical macroglial and microglial responses. Overall, the data to date strongly suggest a heretofore unrecognized, natural checkpoint between retinal deafferentiation and RPE and Müller cell remodeling events. As we continue to discover them, the unique ways by which ground squirrel retina responds to hibernation or injury may be adaptable to therapeutic use. Highlights: Ground squirrels are highly visual hibernators and have a retina with 85% cones. Cone and brain synapses reversibly remodel during winter torpor. After retinal detachment and widespread cone death, reactive gliosis is attenuated. This natural attenuation may be relevant for candidate therapies.