Relative contributions of rod and cone bipolar cell inputs to AII amacrine cell light responses in the mouse retina

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.

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Reconvergence of a rod signal to an AII amacrine cell through divergence to a pair of rod bipolar cells in the mouse retina

Neuroscience Research ◽

10.1016/j.neures.2011.07.293 ◽

2011 ◽

Vol 71 ◽

pp. e69

Author(s):

Yoshihiko Tsukamoto ◽

Naoko Omi

Keyword(s):

Amacrine Cell ◽

Bipolar Cells ◽

Mouse Retina ◽

Rod Bipolar Cells ◽

Aii Amacrine

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

Journal of Neurophysiology ◽

10.1152/jn.00384.2013 ◽

2013 ◽

Vol 110 (9) ◽

pp. 2113-2128 ◽

Cited By ~ 13

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.

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The somal patterning of the AII amacrine cell mosaic in the mouse retina is indistinguishable from random simulations matched for density and constrained by soma size

Visual Neuroscience ◽

10.1017/s0952523817000347 ◽

2018 ◽

Vol 35 ◽

Cited By ~ 1

Author(s):

PATRICK W. KEELEY ◽

BENJAMIN E. REESE

Keyword(s):

Amacrine Cell ◽

Amacrine Cells ◽

Bipolar Cells ◽

Horizontal Cells ◽

Mouse Retina ◽

Retinal Neurons ◽

Soma Size ◽

Aii Amacrine Cells ◽

Aii Amacrine ◽

Cholinergic Amacrine Cells

AbstractThe orderly spacing of retinal neurons is commonly regarded as a characteristic feature of retinal nerve cell populations. Exemplars of this property include the horizontal cells and the cholinergic amacrine cells, where individual cells minimize the proximity to like-type neighbors, yielding regularity in the patterning of their somata. Recently, two types of retinal bipolar cells in the mouse retina were shown to exhibit an order in their somal patterning no different from density-matched simulations constrained by soma size but being otherwise randomly distributed. The present study has now extended this finding to a type of retinal amacrine cell, the AII amacrine cell. Voronoi domain analysis revealed the patterning in the population of AII amacrine somata to be no different from density-matched and soma-size-constrained random simulations, while analysis of the density recovery profile showed AII amacrine cells to exhibit a minimal intercellular spacing identical to that for those random simulations: AII amacrine somata were positioned side-by-side as often as chance would predict. Regularity indexes and packing factors (PF) were far lower than those achieved by either the horizontal cells or cholinergic amacrine cells, with PFs also being comparable to those derived from the constrained random simulations. These results extend recent findings that call into question the widespread assumption that all types of retinal neurons are assembled as regular somal arrays, and have implications for the way in which AII amacrine cells must distribute their processes to ensure a uniform coverage of the retinal surface.

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Intrinsic bursting of AII amacrine cells underlies oscillations in the rd1 mouse retina

Journal of Neurophysiology ◽

10.1152/jn.00437.2014 ◽

2014 ◽

Vol 112 (6) ◽

pp. 1491-1504 ◽

Cited By ~ 49

Author(s):

Hannah Choi ◽

Lei Zhang ◽

Mark S. Cembrowski ◽

Carl F. Sabottke ◽

Alexander L. Markowitz ◽

...

Keyword(s):

Amacrine Cell ◽

Ganglion Cells ◽

Wild Type Mouse ◽

Amacrine Cells ◽

Bipolar Cells ◽

Membrane Properties ◽

Mouse Retina ◽

Intrinsic Membrane Properties ◽

Rd1 Mouse ◽

Aii Amacrine

In many forms of retinal degeneration, photoreceptors die but inner retinal circuits remain intact. In the rd1 mouse, an established model for blinding retinal diseases, spontaneous activity in the coupled network of AII amacrine and ON cone bipolar cells leads to rhythmic bursting of ganglion cells. Since such activity could impair retinal and/or cortical responses to restored photoreceptor function, understanding its nature is important for developing treatments of retinal pathologies. Here we analyzed a compartmental model of the wild-type mouse AII amacrine cell to predict that the cell's intrinsic membrane properties, specifically, interacting fast Na and slow, M-type K conductances, would allow its membrane potential to oscillate when light-evoked excitatory synaptic inputs were withdrawn following photoreceptor degeneration. We tested and confirmed this hypothesis experimentally by recording from AIIs in a slice preparation of rd1 retina. Additionally, recordings from ganglion cells in a whole mount preparation of rd1 retina demonstrated that activity in AIIs was propagated unchanged to elicit bursts of action potentials in ganglion cells. We conclude that oscillations are not an emergent property of a degenerated retinal network. Rather, they arise largely from the intrinsic properties of a single retinal interneuron, the AII amacrine cell.

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