The output from the retina comprises the activity of 10-15 distinct classes of retinal ganglion cells, each optimized for specific spatial and temporal properties. Information transfer over the limited bandwidth available to retinal neurons is optimized by mechanisms that remove redundant information. One hypothesis for such a mechanism is predictive coding, which collects luminance signals from the surrounding regions and subtracts them from the center response, thereby removing correlations, and enhancing the signal-to-noise ratio and transmission of information. We hypothesize that predictive coding can also be implemented by the subtraction of more complex statistics such as contrast, color, motion, or orientation. Surround antagonism, generated first in the outer retina by horizontal cell feed-back onto photoreceptors, propagates to bipolar cells and therefore must be inherent in all ganglion and amacrine cells, but there it is mixed with a surround generated from the inner retina. Feedback from amacrine cells onto bipolar cell terminals and feed-forward from amacrine cells onto a ganglion cell's dendrites endow its surround with non-linear properties. Both outer and inner retinal surrounds are fundamental for the function of vision, but their relative roles are unknown. We pro- pose to test several hypotheses about amacrine and ganglion cell surrounds. We will record from live amacrine and ganglion cells, measure the spatio-temporal extent of their inner and outer retinal surrounds, and using blockers of neurotransmitters GABA and glycine, distinguish between the linear and nonlinear surround properties. We will test the hypothesis that feedback onto a bipolar cell's terminals produces surround inhibition common to more than one postsynaptic ganglion cell type. Second, we will determine which complex receptive field properties unique to a specific ganglion cell type are mediated by feed-forward inhibition. Third, we will study receptive field properties of specific amacrine cell types to determine whether they can convey the nonlinear properties observed in ganglion cells. The experiments will focus on 2 well-characterized concentric ganglion cells, the brisk-transient (BT) and brisk-sustained (BS) cells, and on 2 well characterized complex ganglion cells, the On-Off direction-selective cells (DSGC), and local-edge-detectors (LED), as well as several types of narrow- and wide-field amacrine cell. This work will collect information about retinal structure and function vital to a better understanding of information processing in the visual system and the brain. It will help to understand better how the eye functions, which will help clinical researchers determine what has gone wrong in many types of eye disease and bioengineers in developing prosthetic retinal devices that more closely match the function of the living retina.

Public Health Relevance

Blindness affects millions of Americans and constitutes a significant cost to public and private health sectors. Development of prosthetic devices that can replace the function of the retina is an avenue of treatment that is being actively pursued. This project will elucidate the properties of neural signals in normal retina, which will allow development of prosthetic devices that can better mimic normal retinal function.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY014888-07
Application #
7822725
Study Section
Biology and Diseases of the Posterior Eye Study Section (BDPE)
Program Officer
Greenwell, Thomas
Project Start
2003-07-01
Project End
2012-04-30
Budget Start
2010-05-01
Budget End
2011-04-30
Support Year
7
Fiscal Year
2010
Total Cost
$377,952
Indirect Cost
Name
Oregon Health and Science University
Department
Ophthalmology
Type
Schools of Medicine
DUNS #
096997515
City
Portland
State
OR
Country
United States
Zip Code
97239
Stincic, Todd L; Keeley, Patrick W; Reese, Benjamin E et al. (2018) Bistratified starburst amacrine cells in Sox2 conditional knockout mouse retina display ON and OFF responses. J Neurophysiol 120:2121-2129
Venkataramani, Sowmya; Taylor, W Rowland (2016) Synaptic Mechanisms Generating Orientation Selectivity in the ON Pathway of the Rabbit Retina. J Neurosci 36:3336-49
Taxidis, Jiannis; Anastassiou, Costas A; Diba, Kamran et al. (2015) Local Field Potentials Encode Place Cell Ensemble Activation during Hippocampal Sharp Wave Ripples. Neuron 87:590-604
Murphy-Baum, Benjamin L; Taylor, W Rowland (2015) The Synaptic and Morphological Basis of Orientation Selectivity in a Polyaxonal Amacrine Cell of the Rabbit Retina. J Neurosci 35:13336-50
Balakrishnan, Veeramuthu; Puthussery, Theresa; Kim, Mean-Hwan et al. (2015) Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina. Neuron 87:563-75
Puthussery, Theresa; Percival, Kumiko A; Venkataramani, Sowmya et al. (2014) Kainate receptors mediate synaptic input to transient and sustained OFF visual pathways in primate retina. J Neurosci 34:7611-21
Venkataramani, Sowmya; Van Wyk, Michiel; Buldyrev, Ilya et al. (2014) Distinct roles for inhibition in spatial and temporal tuning of local edge detectors in the rabbit retina. PLoS One 9:e88560
Puthussery, Theresa; Venkataramani, Sowmya; Gayet-Primo, Jacqueline et al. (2013) NaV1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. J Neurosci 33:16045-59
Buldyrev, Ilya; Taylor, W Rowland (2013) Inhibitory mechanisms that generate centre and surround properties in ON and OFF brisk-sustained ganglion cells in the rabbit retina. J Physiol 591:303-25
Vaney, David I; Sivyer, Benjamin; Taylor, W Rowland (2012) Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci 13:194-208

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