A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates

Grimes, William N.; Graves, Logan R; Summers, Mathew T.; Rieke, Fred

doi:10.7554/elife.08033

Cited by 25 publications

(39 citation statements)

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“…As discussed above, this is supported by the observation that the surround is present at the level of the bipolar cell, and therefore at least some portion of the surround enters the circuit before the nonlinearity at the bipolar cell synapse. A rectified bipolar cell synaptic nonlinearity has been well described in the retina [31,37,49,38], including at the output synapse of diffuse cone bipolar cells in primate retina [50,43].…”

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confidence: 99%

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

Turner

Schwartz²

2018

Preprint

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SummaryAlmost every neuron in the early visual system has some form of an antagonistic receptive field surround. But the function of the surround is poorly understood, especially under naturalistic stimulus conditions. Anatomical and functional characterization of the surround of retinal ganglion cells suggests that surround signals combine with the excitatory feedforward pathway upstream of an important synaptic nonlinearity between bipolar cells and postsynaptic ganglion cells. This circuit architecture suggests at least two unexplored consequences for receptive field structure. First, center and surround inputs should interact nonlinearly, even prior to the summation across visual space that forms the full receptive field center. Second, inputs to the surround may alter the sensitivity of the center to spatial contrast in a scene. We test these hypotheses using both synthetic and naturalistic visual stimuli, and find that the statistics of natural scenes promote these nonlinear interactions. This work shows that, unexpectedly, the surround modulates spatial contrast encoding based on visual context.

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confidence: 99%

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

Turner

Schwartz²

2018

Preprint

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“…RBCs form a dyad synapse with the glycinergic AII and GABAergic A17. The A17 forms a reciprocal feedback synapse onto the RBC, releasing GABA onto GABAc and GABAA receptors (Grimes et al, 2015). This shapes the time course of glutamate release from RBCs (Dong & Hare, 2003;Singer & Diamond, 2003;Chavez et al, 2010).…”

Section: Serial Inhibitionmentioning

confidence: 99%

“…The A17 inhibits the RBC though feedback GABA release on the GABA receptors in the RBC terminal. Excessive GABAA or GABAc activation at the rod bipolar cell has been shown to decrease ON GC responsiveness to light in salamander (Ichinose and Lukasiewicz, 2002) and mice (Grimes et al, 2015). The A17- Dopamine acts through D1 receptors to modulate gap junction coupling and extend the dynamic range of light processing.…”

Section: Trpv1 Likely Enhances Sensitivity In the Rod Pathway Via Amamentioning

confidence: 99%

“…In contrast, GABAc responds more slowly and the duration of the response lasts tens to hundreds of milliseconds (Chang & Weiss, 1999;McCall et al, 2002). Tonic A17-mediated GABA release in the dark likely decreases spontaneous glutamate release from RBCs, a process that enhances the signal to noise ratio to dim light at the visual threshold (Grimes et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Further complicating matters, however, is the idea that the responses within these pathways may not be static, but depend on stimulus (Umino et al, 2008;Eggers et al, 2013;Farrow et al, 2013;Grimes et al, 2015). For example, some ON GCs can signal light offset and OFF GCs can signal light onset depending on luminance conditions or stimulus size (Sagdullaev & McCall, 2005;TikidjiHamburyan et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Transient receptor potential cation channel, subfamilies V, member 1 (TRPV1) and M, member 1 (TRPM1) contribute to neural signaling in mouse retina.

Noel¹

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Transient receptor potential cation channel, subfamilies V, member 1 (TRPV1) and M, member 1 (TRPM1) contribute to neural signaling in mouse retina. Jennifer Noel University of LouisvilleFollow this and additional works at: https://ir.library.louisville.edu/etd Part of the Biology Commons, and the Molecular and Cellular Neuroscience CommonsThis Doctoral Dissertation is brought to you for free and open access by ThinkIR: The University of Louisville's Institutional Repository. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of ThinkIR: The University of Louisville's Institutional Repository. This title appears here courtesy of the author, who has retained all other copyrights. For more information, please contact thinkir@louisville.edu. Recommended CitationNoel, Jennifer, "Transient receptor potential cation channel, subfamilies V, member 1 (TRPV1) and M, member 1 (TRPM1) contribute to neural signaling in mouse retina." (2016) Trp channels modulate the responses of retinal neurons within specific pathways..The study of the expression and function of the majority of Trp channels in the retina is largely in its infancy. My dissertation first investigated the expression and function of the transient receptor potential vanilloid-1 (TRPV1) receptor/channel in the retina. TRPV1, the first cloned and most highly studiedTrp channel in the peripheral nervous system, is a non-selective cation channel with an affinity for Ca 2+ . The channel can be activated by capsaicin, acid, endovanilloids, noxious heat or pressure (Moreira et al., 2012). Located on the peripheral and central terminals of nociceptive fibers in the PNS and in limited areas of the CNS (Cavanaugh et al, 2011b). TRPV1 plays a role in inflammation, chronic pain, nociceptor sensitization and desensitization, long-term depression vi and potentiation, and apoptosis. The role of TRPV1 in the retina is not known.Using the electroretinogram (ERG), a mass potential that assesses the function of photoreceptors and bipolar cells, the TRPV1 knockout mouse appears normal.However, TRPV1 is thought to play a role in calcium regulation and glaucoma (Sappington et al., 2009& Leonelli et al., 2010 so we investigated its role in normal visual transduction in the inner retina. To investigate TRPV1 modulation, Irecorded GC spiking responses to light stimuli from mice which either express or lack TRPV1 protein. I found that TRPV1 is critical for:1. GC responses to dim light. Sustained responses to light3. Surround suppression of GCs to large spots. (LRIT3), a novel protein component in the mGluR6-TRPM1 signalplex that was found mutated within cCSNB patients and a knockout mouse (Zeitz et al., 2013; Neuillé et al., 2014). The function of LRIT3 within the cascade remains unknown.To better understand the role of LRIT3, we examined retinal structure and function. We compared the structure of the pre and postsynaptic elements in the OPL of WT and Lrit3 -/-mice using a variety of antibodies and with confocal microscopy. We as...

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Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Kuo

Schwartz

Rieke

2016

Neuron

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102

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Summary Electrical and chemical synapses coexist in circuits throughout the CNS. Yet, it is not well understood how electrical and chemical synaptic transmission interact to determine the functional output of networks endowed with both types of synapse. We found that release of glutamate from bipolar cells onto retinal ganglion cells (RGCs) was strongly shaped by gap junction-mediated electrical coupling within the bipolar cell network of the mouse retina. Specifically, electrical synapses spread signals laterally between bipolar cells, and this lateral spread contributed to a nonlinear enhancement of bipolar cell output to visual stimuli presented closely in space and time. Our findings thus (1) highlight how electrical and chemical transmission can work in concert to influence network output, and (2) reveal a previously unappreciated circuit mechanism that increases RGC sensitivity to spatiotemporally correlated input, such as that produced by motion.

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A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates

Cited by 25 publications

References 22 publications

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

Transient receptor potential cation channel, subfamilies V, member 1 (TRPV1) and M, member 1 (TRPM1) contribute to neural signaling in mouse retina.

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

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