Range, routing and kinetics of rod signaling in primate retina

Grimes, William N.; Baudin, Jacob; Azevedo, Anthony W.

doi:10.7554/elife.38281

Cited by 46 publications

(73 citation statements)

References 67 publications

(116 reference statements)

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“…Notably, in macaque, direct rod-to-Off-CBC input occurs less frequently than in mouse, a result that may explain the lower contribution of the tertiary rod pathway to scotopic signaling in primates (Grimes et al, 2018a).…”

Section: The Primary Rod Pathway Utilizes Specific Off-cbc Circuitsmentioning

confidence: 96%

“…A recent study showed that primates differ from other species in that rod signals are routed principally through the primary rod pathway, via AII-ACs, even at mesopic light levels (Grimes et al, 2018a). However, it is not known whether all of the five primate Off-CBC types (Boycott and Wässle, 1991;Haverkamp et al, 2003;Puthussery et al, 2013Puthussery et al, , 2014Peng et al, 2019) receive AII -AC input, and thus participate in primary rod pathway signaling.…”

Section: Introductionmentioning

confidence: 99%

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

McLaughlin

Percival

Gayet-Primo

et al. 2020

Preprint

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Adapting 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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Section: The Primary Rod Pathway Utilizes Specific Off-cbc Circuitsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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

McLaughlin

Percival

Gayet-Primo

et al. 2020

Preprint

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“…Specifically, the assumption is that the rod bipolar pathway dominates at low mesopic light levels and the (assumed faster) rodcone pathway, mediated by gap junctions between rods and cones, contributes substantially at high mesopic light levels (Figure 2). Our recent work (Grimes et al, 2018a) suggests that this is not the case, and that instead rod signals traverse the primate retina primarily through the rod bipolar pathway across light levels.…”

Section: Dynamic Temporal Delaysmentioning

confidence: 96%

“…First, many rod-cone interactions likely involve both retinal and cortical circuits, and isolating the contributions of each circuit can be difficult (Grimes et al, 2015). Second, it is difficult to generalize between rod-cone interactions in primates and rodents due to differences in visually-guided behavior, in the architecture and cellular composition of retinal circuits, and in the routing of signals through those circuits (Grimes, Baudin, Azevedo, & Rieke, 2018a).…”

Section: Linking the Mechanisms Controlling Parallel Neural Processinmentioning

confidence: 99%

Rod-cone signal interference in the retina shapes perception in primates

Songco-Aguas

Grimes

2019

Preprint

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Linking the activity of neurons, circuits and synapses to human behavior is a fundamental goal of neuroscience. Meeting this goal is challenging, in part because behavior, particularly perception, often masks the complexity of the underlying neural circuits, and in part because of the significant behavioral differences between primates and animals like mice and flies in which genetic manipulations are relatively common. Here we relate circuit-level processing of rod and cone signals in the non-human primate retina to a known break in the normal seamlessness of human vision -a surprising inability to see high contrast flickering lights under specific conditions. We use electrophysiological recordings and perceptual experiments to identify key mechanisms that shape the retinal integration of rod-and cone-generated retinal signals. We incorporate these mechanistic insights into a predictive model that accurately captures the cancellation of rod-and cone-mediated responses and can explain the perceptual insensitivity to flicker.

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“…Three GC types in the mouse retina receive input from the RB pathway at or near visual threshold: the ON α GC and the OFF α and δ GCs, which exhibit high sensitivity to spatial contrast in the visual scene—similar to primate parasol cells —and project to the geniculo-cortical pathway (Ala-Laurila et al, 2011; Ala-Laurila and Rieke, 2014; Dunn et al, 2006; Grimes et al, 2018a; Grimes et al, 2015; Grimes et al, 2014b; Grimes et al, 2018b; Ke et al, 2014; Kuo et al, 2016; Murphy and Rieke, 2006, 2008). Input from the RB pathway to ON α GCs provides the signal that guides behavior at visual threshold (Smeds et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Connectomic analysis reveals an interneuron with an integral role in the retinal circuit for night vision

Park

Lieberman

et al. 2020

Preprint

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18Blindness to Yale University. We thank Tim Maugel and the Laboratory for Biological 19 Ultrastructure (Department of Biology, UMD) for assistance with transmission electron 20 microscopy, Alexander Baden for assistance with 3D visualization, and Kacie Furcolo and Adit 21 Sabnis for assistance with SBEM dataset skeletonization. We thank Cole Graydon for 22 comments on the manuscript. 24 Summary 31The mammalian rod bipolar (RB) cell pathway is perhaps the best-studied circuit in the 32 vertebrate retina. Its synaptic interactions with other retinal circuits, however, remain 33 unresolved. Here, we combined anatomical and physiological analyses of the mouse retina to 34 discover that the majority of synaptic inhibition to the AII amacrine cell (AC), the central neuron 35 in the RB pathway, is provided by a single interneuron type: a multistratified, axon-bearing 36 GABAergic AC, with dendrites in both ON and OFF synaptic layers, but with a pure ON 37 (depolarizing) response to light. We used the nNOS-CreER mouse retina to confirm the identity 38 of this interneuron as the wide-field NOS-1 AC. Our study demonstrates generally that novel 39 neural circuits can be identified from targeted connectomic analyses and specifically that the 40 NOS-1 AC mediates long-range inhibition during night vision and is a major element of the RB 41 pathway. 42 43 74 remain. Most significantly, we do not know the identity of the spiking, GABAergic AC that drives 75 a receptive field surround in the AII during rod-mediated vision via synaptic inhibition of the AII 76 itself (Bloomfield and Xin, 2000); understanding mechanisms contributing to surround inhibition 77 4 is important because such inhibition tunes AII responses to spatial features of the visual 78 stimulus. 79Here, we identified the major inhibitory input to the AII by combining anatomical, genetic, 80 and electrophysiological analyses in a three-step process. One, we reconstructed ACs that 81 provided synaptic input to AIIs in a volume of mouse retina imaged by scanning block-face 82 electron microscopy [SBEM; (Denk and Horstmann, 2004)]. Two, we evaluated published 83 descriptions of reporter mouse lines to identify genetically-accessible ACs that had the 84 anatomical characteristics of the cells reconstructed from SBEM images. And three, we used 85 electrophysiological recordings and genetics-based circuit analysis to demonstrate that a 86 candidate AC, which provided the great majority of the inhibitory synaptic input to AIIs, exhibited 87 a light response predicted by its anatomy and made GABAergic synapses onto AIIs. This 88 spiking, GABAergic AC is a multistratified, ON AC denoted NOS-1 AC and identified in the 89 nNOS-CreER mouse (Zhu et al., 2014). We conclude that the NOS-1 AC is an integral 90 component of the RB pathway and a significant source of long-range inhibition during night 91 vision. More generally, our study demonstrates the utility of targeted, small-scale "connectomic" 92 analysis for identification of novel neural circuits. 94 Results 95AIIs in the ...

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Range, routing and kinetics of rod signaling in primate retina

Cited by 46 publications

References 67 publications

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

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

Rod-cone signal interference in the retina shapes perception in primates

Connectomic analysis reveals an interneuron with an integral role in the retinal circuit for night vision

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