Receptive Fields of Retinal Bipolar Cells Are Mediated by Heterogeneous Synaptic Circuitry

Zhang, Ai Jun; Wu, Samuel M.

doi:10.1523/jneurosci.4984-08.2009

Cited by 59 publications

(77 citation statements)

References 31 publications

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“…4E). Many GABAergic amacrine cells mediate wide inhibitory surrounds (Dacey et al 2000;Ichinose and Lukasiewicz 2005;Sinclair et al 2004;Zhang and Wu 2009) and can be coupled and/or fire action potentials to further extend their spatial signaling (Cook and Werblin 1994;Heflin and Cook 2007;Volgyi et al 2009). Isolated GABAergic input was wider than total input (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…Photoreceptor light information is sent to bipolar cells that synapse onto ganglion cells, the output neurons of the retina, and inhibitory amacrine cells, which shape bipolar cell-ganglion cell signaling (Dong and Werblin 1998;Eggers and Lukasiewicz 2010;2006b;Eggers et al 2007;Sagdullaev et al 2006) by releasing either glycine or GABA (Kolb 1997;Menger et al 1998;Goebel 1985, 1983;Vaney 1990). Morphologically wide GABAergic amacrine cells (Pourcho and Goebel 1983) are thought to primarily carry wide lateral information for center-surround receptive fields (Dacey et al 2000;Ichinose and Lukasiewicz 2005;Sinclair et al 2004;Zhang and Wu 2009), whereas narrow glycinergic amacrine cells (Pourcho and Goebel 1985) provide inhibition between different pathways (Mazade and Eggers 2013;Molnar et al 2009;. However, glycinergic amacrine cells, such as the AII amacrine cell of the rod pathway can be highly coupled, depending on the light state, to extend the spread of their signaling .…”

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confidence: 99%

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Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

Mazade

Eggers

2016

Journal of Neurophysiology

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

Mazade

Eggers

2016

Journal of Neurophysiology

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“…We found that a high dose has devastating side effects on the retina, and thus carefully calibrated the dose and found that 100 μM suppresses the gap junction and enables partial recovery after washing in retinal slices. This dose was used in tiger salamander retinal slices (67) and in mouse retinal slices in this study. Ocular hypertension were induced on the right eye of the C57BL6J mouse line with one of two methods, as follows.…”

Section: Methodsmentioning

confidence: 99%

Elevated intraocular pressure decreases response sensitivity of inner retinal neurons in experimental glaucoma mice

Pang

Frankfort

Gross

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Glaucoma is the second leading cause of blindness in the United States and the world, characterized by progressive degeneration of the optic nerve and retinal ganglion cells (RGCs). Glaucoma patients exhibit an early diffuse loss of retinal sensitivity followed by focal loss of RGCs in sectored patterns. Recent evidence has suggested that this early sensitivity loss may be associated with dysfunctions in the inner retina, but detailed cellular and synaptic mechanisms underlying such sensitivity changes are largely unknown. In this study, we use whole-cell voltage-clamp techniques to analyze light responses of individual bipolar cells (BCs), AII amacrine cells (AIIACs), and ON and sustained OFF alpha-ganglion cells (ONαGCs and sOFFαGCs) in dark-adapted mouse retinas with elevated intraocular pressure (IOP). We present evidence showing that elevated IOP suppresses the rod ON BC inputs to AIIACs, resulting in less sensitive AIIACs, which alter AIIAC inputs to ONαGCs via the AIIAC→cone ON BC→ONαGC pathway, resulting in lower ONαGC sensitivity. The altered AIIAC response also reduces sOFFαGC sensitivity via the AIIAC→sOFFαGC chemical synapses. These sensitivity decreases in αGCs and AIIACs were found in mice with elevated IOP for 3-7 wk, a stage when little RGC or optic nerve degeneration was observed. Our finding that elevated IOP alters neuronal function in the inner retina before irreversible structural damage occurs provides useful information for developing new diagnostic tools and treatments for glaucoma in human patients.laucoma is a leading cause of irreversible blindness in the United States and the world (1, 2), and is characterized by optic nerve cupping (thinning of the neuroretinal rim at the optic nerve head) and progressive optic nerve and retinal ganglion cell (RGC) degeneration as well as functional deficit revealed by psychophysical tests (3, 4). Although factors causing the eventual RGC death and blindness remain controversial (1, 5-8), increasing evidence from human patients and animal models has shown that the disease is associated with an early mild diffuse loss of retinal sensitivity or inner retinal response decrease (9-14). Although it is unclear whether these functional changes are a prelude or even causal to RGC death and blindness, elucidating the underlying synaptic and cellular mechanisms for such sensitivity/response decline will nevertheless provide novel insights pertaining to early detection and treatment of human glaucoma.Multiple risk factors are associated with glaucomatous diseases, among which elevated intraocular pressure (IOP) is widely accepted as the most significant for both disease onset and progression (2, 15). Because high IOP (H-IOP) is an important risk factor, many experimental animal models of elevated IOP have been developed in multiple species including monkeys, rats, and mice (16)(17)(18)(19)(20)(21)(22). Most experiments performed in animal models have focused on anatomical and histopathological analyses of RGC death, axon loss, and changes to axonal projections ...

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“…Light sensitivity varies among subsets of ON cone bipolar cells, which is attributable to the mixed inputs from rods and cones (Pang et al, 2004(Pang et al, , 2010. The effect of surround inhibition on visual signaling is diverse among bipolar cell subsets (Molnar and Werblin, 2007;Zhang and Wu, 2009). Chromatic responses have been shown to be bipolar cell subtype dependent (Haverkamp et al, 2005;Breuninger et al, 2011).…”

Section: Bipolar Cell Subtypes and Functionsmentioning

confidence: 99%

Roles of ON Cone Bipolar Cell Subtypes in Temporal Coding in the Mouse Retina

Ichinose

Fyk‐Kolodziej

Cohn

2014

Journal of Neuroscience

112

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In the visual system, diverse image processing starts with bipolar cells, which are the second-order neurons of the retina. Thirteen subtypes of bipolar cells have been identified, which are thought to encode different features of image signaling and to initiate distinct signal-processing streams. Although morphologically identified, the functional roles of each bipolar cell subtype in visual signal encoding are not fully understood. Here, we investigated how ON cone bipolar cells of the mouse retina encode diverse temporal image signaling. We recorded bipolar cell voltage changes in response to two different input functions: sinusoidal light and step light stimuli. Temporal tuning in ON cone bipolar cells was diverse and occurred in a subtype-dependent manner. Subtypes 5s and 8 exhibited low-pass filtering property in response to a sinusoidal light stimulus, and responded with sustained fashion to step-light stimulation. Conversely, subtypes 5f, 6, 7, and XBC exhibited bandpass filtering property in response to sinusoidal light stimuli, and responded transiently to step-light stimuli. In particular, subtypes 7 and XBC were high-temporal tuning cells. We recorded responses in different ways to further examine the underlying mechanisms of temporal tuning. Current injection evoked low-pass filtering, whereas light responses in voltage-clamp mode produced bandpass filtering in all ON bipolar cells. These findings suggest that cone photoreceptor inputs shape bandpass filtering in bipolar cells, whereas intrinsic properties of bipolar cells shape low-pass filtering. Together, our results demonstrate that ON bipolar cells encode diverse temporal image signaling in a subtype-dependent manner to initiate temporal visual information-processing pathways.

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Receptive Fields of Retinal Bipolar Cells Are Mediated by Heterogeneous Synaptic Circuitry

Cited by 59 publications

References 31 publications

Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

Elevated intraocular pressure decreases response sensitivity of inner retinal neurons in experimental glaucoma mice

Roles of ON Cone Bipolar Cell Subtypes in Temporal Coding in the Mouse Retina

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