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 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 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.

Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina

1999 ◽  
Vol 16 (6) ◽  
pp. 1181-1189 ◽  
Author(s):  
STEPHEN C. MASSEY ◽  
STEPHEN L. MILLS
Keyword(s):  
Gap Junctions ◽  
Bipolar Cell ◽  
Amacrine Cells ◽  
Positive Cone ◽  
Bipolar Cells ◽  
Cell Network ◽  
Ribbon Synapses ◽  
Aii Amacrine Cells ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

Electrical synapses or gap junctions occur between many retinal neurons. However, in most cases, the gap junctions have not been visualized directly. Instead, their presence has been inferred from tracer spread throughout the network of cells. Thus, tracer coupling is taken as a marker for the presence of gap junctions between coupled cells. AII amacrine cells are critical interneurons in the rod pathway of the mammalian retina. Rod bipolar cell output passes to AII amacrine cells, which in turn make conventional synapses with OFF cone bipolar cells and gap junctions with ON cone bipolar cells. Injections of biotinylated tracers into AII amacrine cells reveals coupling between the AII amacrine cell network and heterologous coupling with a variety of ON cone bipolar cells, including the calbindin-positive cone bipolar cell. To directly visualize gap junctions in this network, we prepared material for electron microscopy that was double labeled with antibodies to calretinin and calbindin to label AII amacrine cells and calbindin-positive cone bipolar cells, respectively. AII amacrine cells were postsynaptic to large vesicle-laden rod bipolar terminals, as previously reported. Gap junctions were identified between AII amacrine cells and calbindin-positive cone bipolar cell terminals identified by the presence of immunostaining and ribbon synapses. This represents direct confirmation of gap junctions between two different yet positively identified cells, which are tracer coupled, and provides additional evidence that tracer coupling with Neurobiotin indicates the presence of gap junctions. These results also definitively establish the presence of gap junctions between AII amacrine cells and calbindin bipolar cells which can therefore carry rod signals to the ON alpha ganglion cell.

Rod signals are routed through specific Off cone bipolar cells in primate retina

2020 ◽  
Author(s):  
Amanda J. McLaughlin ◽  
Kumiko A. Percival ◽  
Jacqueline Gayet-Primo ◽  
Teresa Puthussery
Keyword(s):  
Bipolar Cell ◽  
Amacrine Cell ◽  
Amacrine Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Visual Signals ◽  
Night Time ◽  
Pass Through ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

AbstractAdapting between scotopic and photopic illumination involves switching the routing of retinal signals between rod and cone-dominated circuits. In the daytime, cone signals pass through parallel On and Off cone bipolar cells, that are sensitive to increments and decrements in luminance, respectively. At night, rod signals are routed into these cone-pathways via a key glycinergic interneuron, the AII amacrine cell (AII-AC). In primates, it is not known whether AII-ACs contact all Off-bipolar cell types indiscriminately, or whether their outputs are biased towards specific Off-bipolar cell types. Here, we show that the rod-driven glycinergic output of AII-ACs is strongly biased towards a subset of macaque Off-cone bipolar cells. The Off-bipolar types that receive this glycinergic input have sustained physiological properties and include the Off-midget bipolar cells, which provide excitatory input to the Off-midget ganglion cells (parvocellular pathway). The kinetics of the glycinergic events are consistent with the involvement of the α1 glycine receptor subunit. Taken together with results in mouse retina, our findings point towards a conserved motif whereby rod signals are preferentially routed into sustained Off signaling pathways.Significance StatementVisual signals pass through different retinal neurons depending on the prevailing level of illumination. Under night-time light levels, signals from rods pass through the AII amacrine cell, an inhibitory interneuron that routes rod signals into On and Off bipolar cells to detect increments and decrements in light intensity, respectively. Here, we show in primate retina that the output of AII amacrine cells is strongly biased towards specific Off bipolar cell types, which suggests that rod signals reach the brain via specific neural channels. Our results further our understanding of how visual signals are routed through visual circuits during night-time vision.

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.

scholarly journals Light adaptation alters the source of inhibition to the mouse retinal OFF pathway

2013 ◽  
Vol 110 (9) ◽  
pp. 2113-2128 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers
Keyword(s):  
Bipolar Cell ◽  
Light Adaptation ◽  
Amacrine Cell ◽  
Bipolar Cells ◽  
Gabaergic Inhibition ◽  
Light Sensing ◽  
Wide Range ◽  
Rod Pathway ◽  
Aii Amacrine ◽  
Cone Bipolar Cells

Sensory systems must avoid saturation to encode a wide range of stimulus intensities. One way the retina accomplishes this is by using both dim-light-sensing rod and bright-light-sensing cone photoreceptor circuits. OFF cone bipolar cells are a key point in this process, as they receive both excitatory input from cones and inhibitory input from AII amacrine cells via the rod pathway. However, in addition to AII amacrine cell input, other inhibitory inputs from cone pathways also modulate OFF cone bipolar cell light signals. It is unknown how these inhibitory inputs to OFF cone bipolar cells change when switching between rod and cone pathways or whether all OFF cone bipolar cells receive rod pathway input. We found that one group of OFF cone bipolar cells (types 1, 2, and 4) receive rod-mediated inhibitory inputs that likely come from the rod-AII amacrine cell pathway, while another group of OFF cone bipolar cells (type 3) do not. In both cases, dark-adapted rod-dominant light responses showed a significant contribution of glycinergic inhibition, which decreased with light adaptation and was, surprisingly, compensated by an increase in GABAergic inhibition. As GABAergic input has distinct timing and spatial spread from glycinergic input, a shift from glycinergic to GABAergic inhibition could significantly alter OFF cone bipolar cell signaling to downstream OFF ganglion cells. Larger GABAergic input could reflect an adjustment of OFF bipolar cell spatial inhibition, which may be one mechanism that contributes to retinal spatial sensitivity in the light.

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.

scholarly journals Random spatial patterning of cone bipolar cell mosaics in the mouse retina

2017 ◽  
Vol 34 ◽  
Author(s):  
PATRICK W. KEELEY ◽  
JASON J. KIM ◽  
SAMMY C.S. LEE ◽  
SILKE HAVERKAMP ◽  
BENJAMIN E. REESE
Keyword(s):  
Bipolar Cell ◽  
Amacrine Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Statistical Properties ◽  
Horizontal Cells ◽  
Mouse Retina ◽  
Dendritic Arbors ◽  
Cone Bipolar Cells ◽  
Cholinergic Amacrine Cells

AbstractRetinal bipolar cells spread their dendritic arbors to tile the retinal surface, extending them to the tips of the dendritic fields of their homotypic neighbors, minimizing dendritic overlap. Such uniform nonredundant dendritic coverage of these populations would suggest a degree of spatial order in the properties of their somal distributions, yet few studies have examined the patterning in retinal bipolar cell mosaics. The present study examined the organization of two types of cone bipolar cells in the mouse retina, the Type 2 cells and the Type 4 cells, and compared their spatial statistical properties with those of the horizontal cells and the cholinergic amacrine cells, as well as to random simulations of cells matched in density and constrained by soma size. The Delauney tessellation of each field was computed, from which nearest neighbor distances and Voronoi domain areas were extracted, permitting a calculation of their respective regularity indexes (RIs). The spatial autocorrelation of the field was also computed, from which the effective radius and packing factor (PF) were determined. Both cone bipolar cell types were found to be less regular and less efficiently packed than either the horizontal cells or cholinergic amacrine cells. Furthermore, while the latter two cell types had RIs and PFs in excess of those for their matched random simulations, the two types of cone bipolar cells had spatial statistical properties comparable to random distributions. An analysis of single labeled cone bipolar cells revealed dendritic arbors frequently skewed to one side of the soma, as would be expected from a randomly distributed population of cells with dendrites that tile. Taken together, these results suggest that, unlike the horizontal cells or cholinergic amacrine cells which minimize proximity to one another, cone bipolar cell types are constrained only by their physical size.

Analysis of two types of cone bipolar cells in the retina of a New World monkey, the marmoset, Callithrix jacchus

1999 ◽  
Vol 16 (4) ◽  
pp. 707-719 ◽  
Author(s):  
XUEGANG LUO ◽  
KRISHNA K. GHOSH ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT
Keyword(s):  
Bipolar Cell ◽  
New World ◽  
Random Distribution ◽  
World Monkey ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
New World Primates ◽  
New World Monkey ◽  
Cone Bipolar Cells

Two types of cone bipolar cells, the blue cone bipolar cell and the diffuse bipolar cell (DB3), were labelled immunohistochemically and investigated in the retina of a New World monkey, the marmoset. Blue cone bipolar cells were labelled with an antiserum against cholecystokinin. Short-wavelength-sensitive (SWS) cones were labelled with an antiserum against the SWS cone opsin. The DB3 cells were labelled with antibodies to calbindin. Blue cone bipolar cells in marmoset do not form a regular mosaic but instead follow the random distribution of the SWS cones. Nevertheless, the SWS cone to blue cone bipolar cell connectivity in marmoset is very similar to that previously described for macaque. In contrast to the blue cone bipolar cells, the DB3 cells form a regular mosaic. The synaptic connectivity of DB3 cells in the inner plexiform layer was analyzed. They make output synapses onto ganglion cells and amacrine cells, and gap junctions with each other. Our results provide further evidence for the existence of parallel bipolar cell pathways in the primate retina and support the view that the retinae of Old World and New World primates have common neuronal connectivity. The random distribution of SWS cones and blue cone bipolar cells is an exception to the general rule of a regular mosaic distribution of cell populations in the retina.

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