scholarly journals Inhibitory components of retinal bipolar cell receptive fields are differentially modulated by dopamine D1 receptors

2020 ◽  
Vol 37 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers
Keyword(s):  
Receptive Field ◽  
Bipolar Cell ◽  
Light Adaptation ◽  
Receptive Fields ◽  
Amacrine Cells ◽  
Receptor Activation ◽  
Bipolar Cells ◽  
D1 Receptor ◽  
D1 Receptors ◽  
Inhibitory Strength

Abstract During adaptation to an increase in environmental luminance, retinal signaling adjustments are mediated by the neuromodulator dopamine. Retinal dopamine is released with light and can affect center-surround receptive fields, the coupling state between neurons, and inhibitory pathways through inhibitory receptors and neurotransmitter release. While the inhibitory receptive field surround of bipolar cells becomes narrower and weaker during light adaptation, it is unknown how dopamine affects bipolar cell surrounds. If dopamine and light have similar effects, it would suggest that dopamine could be a mechanism for light-adapted changes. We tested the hypothesis that dopamine D1 receptor activation is sufficient to elicit the magnitude of light-adapted reductions in inhibitory bipolar cell surrounds. Surrounds were measured from OFF bipolar cells in dark-adapted mouse retinas while stimulating D1 receptors, which are located on bipolar, horizontal, and inhibitory amacrine cells. The D1 agonist SKF-38393 narrowed and weakened OFF bipolar cell inhibitory receptive fields but not to the same extent as with light adaptation. However, the receptive field surround reductions differed between the glycinergic and GABAergic components of the receptive field. GABAergic inhibitory strength was reduced only at the edges of the surround, while glycinergic inhibitory strength was reduced across the whole receptive field. These results expand the role of retinal dopamine to include modulation of bipolar cell receptive field surrounds. Additionally, our results suggest that D1 receptor pathways may be a mechanism for the light-adapted weakening of glycinergic surround inputs and the furthest wide-field GABAergic inputs to bipolar cells. However, remaining differences between light-adapted and D1 receptor–activated inhibition demonstrate that non-D1 receptor mechanisms are necessary to elicit the full effect of light adaptation on inhibitory surrounds.

scholarly journals Dopamine D1 receptor activation reduces local inner retinal inhibition to light-adapted levels

2019 ◽  
Vol 121 (4) ◽  
pp. 1232-1243 ◽  
Author(s):  
Reece E. Mazade ◽  
Michael D. Flood ◽  
Erika D. Eggers
Keyword(s):  
Bipolar Cell ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Receptor Activation ◽  
Bipolar Cells ◽  
D1 Receptor ◽  
D1 Receptors ◽  
Local Inhibition ◽  
Local Circuits ◽  
Cone Bipolar Cells

During adaptation from dim to bright environments, changes in retinal signaling are mediated, in part, by dopamine. Dopamine is released with light and can modulate retinal receptive fields, neuronal coupling, inhibitory receptors, and rod pathway inhibition. However, it is unclear how dopamine affects inner retinal inhibition to cone bipolar cells, which relay visual information from photoreceptors to ganglion cells and are important signal processing sites. We tested the hypothesis that dopamine (D)1 receptor activation is sufficient to elicit light-adapted inhibitory changes. Local light-evoked inhibition and spontaneous activity were measured from OFF cone bipolar cells in dark-adapted mouse retinas while stimulating D1 receptors, which are located on bipolar, horizontal, and inhibitory amacrine cells. The D1 agonist SKF38393 reduced local inhibitory light-evoked response magnitude and increased response transience, which mimicked changes measured with light adaptation. D1-mediated reductions in local inhibition were more pronounced for glycinergic than GABAergic inputs, comparable with light adaptation. The effects of D1 receptors on light-evoked input were similar to the effects on spontaneous input. D1 receptor activation primarily decreased glycinergic spontaneous current frequency, similar to light adaptation, suggesting mainly a presynaptic amacrine cell site of action. These results expand the role of dopamine to include signal modulation of cone bipolar cell local inhibition. In this role, D1 receptor activation, acting primarily through glycinergic amacrine cells, may be an important mechanism for the light-adapted reduction in OFF bipolar cell inhibition since the actions are similar and dopamine is released during light adaptation. NEW & NOTEWORTHY Retinal adaptation to different luminance conditions requires the adjustment of local circuits for accurate signaling of visual scenes. Understanding mechanisms behind luminance adaptation at different retinal levels is important for understanding how the retina functions in a dynamic environment. In the mouse, we show that dopamine pathways reduce inner retinal inhibition similar to increased background luminance, suggesting the two are linked and highlighting a possible mechanism for light adaptation at an early retinal processing center.

scholarly journals Dopamine D1 receptor activation contributes to light-adapted changes in retinal inhibition to rod bipolar cells

2018 ◽  
Vol 120 (2) ◽  
pp. 867-879 ◽  
Author(s):  
Michael D. Flood ◽  
Johnnie M. Moore-Dotson ◽  
Erika D. Eggers
Keyword(s):  
Light Adaptation ◽  
Amacrine Cell ◽  
Amacrine Cells ◽  
Receptor Activation ◽  
Bipolar Cells ◽  
D1 Receptor ◽  
D1 Receptors ◽  
Light Responses ◽  
Dopamine Modulation ◽  
Rod Bipolar Cells

Dopamine modulation of retinal signaling has been shown to be an important part of retinal adaptation to increased background light levels, but the role of dopamine modulation of retinal inhibition is not clear. We previously showed that light adaptation causes a large reduction in inhibition to rod bipolar cells, potentially to match the decrease in excitation after rod saturation. In this study, we determined how dopamine D1 receptors in the inner retina contribute to this modulation. We found that D1 receptor activation significantly decreased the magnitude of inhibitory light responses from rod bipolar cells, whereas D1 receptor blockade during light adaptation partially prevented this decline. To determine what mechanisms were involved in the modulation of inhibitory light responses, we measured the effect of D1 receptor activation on spontaneous currents and currents evoked from electrically stimulating amacrine cell inputs to rod bipolar cells. D1 receptor activation decreased the frequency of spontaneous inhibition with no change in event amplitudes, suggesting a presynaptic change in amacrine cell activity in agreement with previous reports that rod bipolar cells lack D1 receptors. Additionally, we found that D1 receptor activation reduced the amplitude of electrically evoked responses, showing that D1 receptors can modulate amacrine cells directly. Our results suggest that D1 receptor activation can replicate a large portion but not all of the effects of light adaptation, likely by modulating release from amacrine cells onto rod bipolar cells. NEW & NOTEWORTHY We demonstrated a new aspect of dopaminergic signaling that is involved in mediating light adaptation of retinal inhibition. This D1 receptor-dependent mechanism likely acts through receptors located directly on amacrine cells, in addition to its potential role in modulating the strength of serial inhibition between amacrine cells. Our results also suggest that another D2/D4 receptor-dependent or dopamine-independent mechanism must also be involved in light adaptation of inhibition to rod bipolar cells.

Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina

1999 ◽  
Vol 16 (4) ◽  
pp. 653-665 ◽  
Author(s):  
DAIYAN XIN ◽  
STEWART A. BLOOMFIELD
Keyword(s):  
Receptive Field ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Rabbit Retina ◽  
Response Component ◽  
Synaptic Inputs ◽  
Field Organization ◽  
Receptive Field Organization ◽  
Aii Amacrine Cells

We studied the light-evoked responses of AII amacrine cells in the rabbit retina under dark- and light-adapted conditions. In contrast to the results of previous studies, we found that AII cells display robust responses to light over a 6–7 log unit intensity range, well beyond the operating range of rod photoreceptors. Under dark adaptation, AII cells showed an ON-center/OFF-surround receptive-field organization. The intensity–response profile of the center-mediated response component followed a dual-limbed sigmoidal function indicating a transition from rod to cone mediation as stimulus intensities were increased. Following light adaptation, the receptive-field organization of AII cells changed dramatically. Light-adapted AII cells showed both ON- and OFF-responses to stimulation of the center receptive field, but we found no evidence for an antagonistic surround. Interestingly, the OFF-center response appeared first following rapid light adaptation and was then replaced gradually over a 1–4 min period by the emerging ON-center response component. Application of the metabotropic glutamate receptor agonist APB, the ionotropic glutamate blocker CNQX, 8-bromo-cGMP, and the nitric oxide donor SNAP all showed differential effects on the various center-mediated responses displayed by dark- and light-adapted AII cells. Taken together, these pharmacological results indicated that different synaptic circuits are responsible for the generation of the different AII cell responses. Specifically, the rod-driven ON-center responses are apparently derived from rod bipolar cell synaptic inputs, whereas the cone-driven ON-center responses arise from signals crossing the gap junctions between AII cells and ON-center cone bipolar cells. Additionally, the OFF-center response of light-adapted AII cells reflects direct synaptic inputs from OFF-center cone bipolar cells to AII dendritic processes in the distal inner plexiform layer.

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

2016 ◽  
Vol 115 (6) ◽  
pp. 2761-2778 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Light Adaptation ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Excitatory Input ◽  
Bipolar Cells ◽  
Visual Sensitivity ◽  
Resting Membrane Potential ◽  
Wide Range

The retina adjusts its signaling gain over a wide range of light levels. A functional result of this is increased visual acuity at brighter luminance levels (light adaptation) due to shifts in the excitatory center-inhibitory surround receptive field parameters of ganglion cells that increases their sensitivity to smaller light stimuli. Recent work supports the idea that changes in ganglion cell spatial sensitivity with background luminance are due in part to inner retinal mechanisms, possibly including modulation of inhibition onto bipolar cells. To determine how the receptive fields of OFF cone bipolar cells may contribute to changes in ganglion cell resolution, the spatial extent and magnitude of inhibitory and excitatory inputs were measured from OFF bipolar cells under dark- and light-adapted conditions. There was no change in the OFF bipolar cell excitatory input with light adaptation; however, the spatial distributions of inhibitory inputs, including both glycinergic and GABAergic sources, became significantly narrower, smaller, and more transient. The magnitude and size of the OFF bipolar cell center-surround receptive fields as well as light-adapted changes in resting membrane potential were incorporated into a spatial model of OFF bipolar cell output to the downstream ganglion cells, which predicted an increase in signal output strength with light adaptation. We show a prominent role for inner retinal spatial signals in modulating the modeled strength of bipolar cell output to potentially play a role in ganglion cell visual sensitivity and acuity.

scholarly journals Center-surround interactions underlie bipolar cell motion sensing in the mouse retina

2021 ◽  
Author(s):  
Sarah Strauss ◽  
Maria M Korympidou ◽  
Yanli Ran ◽  
Katrin Franke ◽  
Timm Schubert ◽  
...  
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Motion Processing ◽  
Local Motion ◽  
Motion Sensing ◽  
Motion Sensitivity

Motion is a critical aspect of vision. We studied the representation of motion in mouse retinal bipolar cells and found, surprisingly, that some bipolar cells possess motion-sensing capabilities that rely on their center-surround receptive fields. Using a glutamate sensor, we directly observed motion-sensitive bipolar cell synaptic output, which was strongest for local motion and dependent on the motion's origin. We characterized bipolar cell receptive fields and found that there are motion and non-motion sensitive bipolar cell types, the majority being motion sensitive. Next, we used these bipolar cell receptive fields along with connectomics to design biophysical models of downstream cells. The models and experiments demonstrated that bipolar cells pass motion-sensitive excitation to starburst amacrine cells through direction-specific signals mediated by bipolar cells' center-surround receptive field structure. As bipolar cells provide excitation to most amacrine and ganglion cells, their motion sensitivity may contribute to motion processing throughout the visual system.

Functional organization of catfish retina

1977 ◽  
Vol 40 (1) ◽  
pp. 26-43 ◽  
Author(s):  
K. Naka
Keyword(s):  
Receptive Field ◽  
Ganglion Cell ◽  
Functional Organization ◽  
Ganglion Cells ◽  
Horizontal Cell ◽  
Receptive Fields ◽  
Amacrine Cells ◽  
Type A ◽  
Bipolar Cells ◽  
The Other

1. The basic organization of the biphasic (or concentric) receptive field is established in the bipolar cells as the result of an interaction between two signals, one local representing the activity of a small number of receptors, and the other integrating (19, 20) or global (28) coming from the S space or a lamina formed by the horizontal cells (8, 14, 22, 29). 2. Bipolar-ganglion cell pairs are segregated into two types; A (on center) and B (off center) pairs. A depolarization of a bipolar cell produces spike discharges from ganglion cells of the same type and a hyperpolarization depresses their discharges. I haven't detected any cross talk between the types A and B pairs. Bipolar and ganglion cells must be interfaced by the classical chemical synapses, the only such kind in the catfish retina. 3. Horizontal and type N neurons form two lateral transmission systems, one distal and the other proximal (19, 20). Signals in the lateral systems are shared by the two receptive-field types and are not excitatory or inhibitory in themselves; it is incumbent upon the postsynaptic neurons to decide the polarity of the synaptic transmission. The horizontal cell participates directly in the formation of biphasic receptive fields of bipolar cells by providing their surrounding, whereas type N neuron seems to modify the receptive-field organization established in the bipolar cells. 4. Type N neurons are amacrine cells because they do not produce spike discharges (2, 18, 21) and because they influence the activity of both A and B receptive fields. 5. The function of the type C neuron is as unique as its structure (21) and is not fully clear as yet. It is not a conventional amacrine cell as the type N appears to be, nor is it a classical ganglion cell which forms either a type A or B receptive field (2). 6. Type Y neurons are a class of ganglion cells which forms either a type A or B receptive field.

Structure of the receptive fields of bipolar cells in the salamander retina

1987 ◽  
Vol 58 (6) ◽  
pp. 1275-1291 ◽  
Author(s):  
S. Borges ◽  
M. Wilson
Keyword(s):  
Receptive Field ◽  
Bipolar Cell ◽  
Synaptic Connection ◽  
Lucifer Yellow ◽  
Receptive Fields ◽  
Bipolar Cells ◽  
Light Scatter ◽  
Small Spot ◽  
Dendritic Arbors ◽  
Rule Out

1. The receptive-field structure of bipolar cells in the salamander retina has been examined using isolated retinae from dark-adapted eyes. 2. Receptive-field mapping was carried out with a 25-microns diam spot of light whose wavelength and intensity was intended to stimulate rods rather than cones. 3. Both hyperpolarizing and depolarizing bipolar cells showed receptive fields having a single central point of maximum sensitivity from which sensitivity declined radially. Antagonistic surrounds could not be demonstrated using a small spot of light. 4. The diameter of receptive fields was found to vary between 374 and 662 micron, consistent with a single bipolar cell being effectively connected to 323-1,275 rods. 5. Lucifer yellow injections of bipolar cells revealed dendritic arbors whose greatest dimensions varied between 43 and 70 microns, consistent with a direct synaptic connection of between 10 and 24 rods to each bipolar cell. 6. We rule out signal spread within the rod network, extensive lateral ramification of rod process, nonlinearity of synaptic transmission, and light scatter, as possible explanations of large bipolar cell receptive fields. It seems likely, instead, that signals are extensively shared between bipolar cells.

Immunocytochemical localization of dopamine D1 receptors in the retina of mammals

1997 ◽  
Vol 14 (3) ◽  
pp. 545-551 ◽  
Author(s):  
J. Nguyen-Legros ◽  
A. Simon ◽  
I. Caillé ◽  
B. Bloch
Keyword(s):  
Bipolar Cell ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Macaque Monkey ◽  
Bipolar Cells ◽  
D1 Receptors ◽  
Rcs Rat ◽  
Severe Impairment ◽  
Displaced Amacrine Cells

AbstractDopamine is one of the major neurotransmitters in the retina. It is released from amacrine and interplexiform cells into both inner (IPL) and outer (OPL) plexiform layers. Several dopaminergic actions are known to occur through D1 receptors (D1R) but the precise location of these receptors has not been established. An antibody that recognizes the intracytoplasmic C-terminal of the rat D1R was used to detect D1R, immunohistochemically, in rats (Wistar and RCS), mouse, hamster, and macaque monkey retinas. The OPL was heavily stained in each species, consistent with the known actions of dopamine on horizontal cells. Three to five bands were observed in the IPL, depending on species. Three were in the a sublayer, the outermost of which was close to the amacrine cell layer, and may represent the massive dopamine input to the AII rod-amacrine cells. As observed in mice, where bipolar cells are D1-immunoreactive, the band located in sublayer 3 of the IPL may contain cone-bipolar cell terminals. A band of D1R-immunoreactivity in the b sublayer of the IPL contains ON-bipolar cell terminals and a second site of interaction between dopaminergic cells and the AII amacrine cells. This sublayer was absent from the RCS rat retina, suggesting a severe impairment of the rod-driven pathway following rod degeneration in these mutant rats. Cells in the ganglion cell layer exhibited relatively heavy staining, and may be ganglion cells or displaced amacrine cells. Some extrasynaptic localizations of D1R in the retina are suggested.

Similar effects of carbachol and dopamine on neurons in the distal retina of the tiger salamander

1995 ◽  
Vol 12 (3) ◽  
pp. 443-455 ◽  
Author(s):  
William A. Hare ◽  
W. Geoffrey Owen
Keyword(s):  
Dopamine Release ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
D1 Receptors ◽  
Ambystoma Tigrinum ◽  
Tiger Salamander ◽  
Retinal Neurons ◽  
D2 Dopamine Receptors

AbstractThough there is considerable evidence that dopamine is an important retinal neuromodulator that mediates many of the changes in the properties of retinal neurons that are normally seen during light adaptation, the mechanism by which dopamine release is controlled remains poorly understood. In this paper, we present evidence which indicates that dopamine release in the retina of the tiger salamander, Ambystoma tigrinum, is driven excitatorily by a cholinergic input. We compared the effects of applying carbachol to those of dopamine application on the responses of rods, horizontal cells, and bipolar cells recorded intracellularly from the isolated, perfused retina of the tiger salamander. Micromolar concentrations of dopamine reduced the amplitudes of rod responses throughout the rods' operating range. The ratio of amplitudes of the cone-driven to rod-driven components of the responses of both horizontal and bipolar cells was increased by activation of both D1 and D2 dopamine receptors. Dopamine acted to uncouple horizontal cells and also off-center bipolar cells, the mechanism in the case of horizontal cells depending only upon activation of D1 receptors. Carbachol, a specific cholinomimetic, applied in five- to ten-fold higher concentrations, produced effects that were essentially identical to those of dopamine. These effects of carbachol were blocked by application of specific dopamine blockers, however, indicating that they are mediated secondarily by dopamine. We propose that the dopamine-releasing amacrine cells in the salamander are under the control of cells, probably amacrine cells, which secrete acetylcholine as their transmitter.

scholarly journals Inhibition to retinal rod bipolar cells is regulated by light levels

2013 ◽  
Vol 110 (1) ◽  
pp. 153-161 ◽  
Author(s):  
Erika D. Eggers ◽  
Reece E. Mazade ◽  
Justin S. Klein
Keyword(s):  
Bipolar Cell ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Significant Inhibition ◽  
Bipolar Cells ◽  
Background Light ◽  
Wide Range ◽  
Cell Inhibition ◽  
Rod Bipolar Cells ◽  
Rod Pathway

The retina responds to a wide range of light stimuli by adaptation of retinal signaling to background light intensity and the use of two different photoreceptors: rods that sense dim light and cones that sense bright light. Rods signal to rod bipolar cells that receive significant inhibition from amacrine cells in the dark, especially from a rod bipolar cell-activated GABAergic amacrine cell. This inhibition modulates the output of rod bipolar cells onto downstream neurons. However, it was not clear how the inhibition of rod bipolar cells changes when rod signaling is limited by an adapting background light and cone signaling becomes dominant. We found that both light-evoked and spontaneous rod bipolar cell inhibition significantly decrease with light adaptation. This suggests a global decrease in the activity of amacrine cells that provide input to rod bipolar cells with light adaptation. However, inhibition to rod bipolar cells is also limited by GABAergic connections between amacrine cells, which decrease GABAergic input to rod bipolar cells. When we removed this serial inhibition, the light-evoked inhibition to rod bipolar cells remained after light adaptation. These results suggest that decreased inhibition to rod bipolar cells after light adaptation is due to decreased rod pathway activity as well as an active increase in inhibition between amacrine cells. Together these serve to limit rod bipolar cell inhibition after light adaptation, when the rod pathway is inactive and modulation of the signal is not required. This suggests an efficiency mechanism in the retina to limit unnecessary signaling.

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