Direction selectivity in retinal bipolar cell axon terminals

Matsumoto, Akira; Agbariah, Weaam; Nolte, Stella Solveig; Andrawos, Rawan; Levi, Hadara; Sabbah, Shai; Yonehara, Keisuke

doi:10.1016/j.neuron.2021.07.008

Cited by 34 publications

(28 citation statements)

References 74 publications

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“…The presence of direction selectivity in a spiking, polyaxonal, amacrine type linked to the recursive bistratified ganglion cell is distinctive but parallels an emerging picture in the non-primate mammal 6 , 69 , 82 , 83 . Direction selectivity in the ON–OFF A1 cell could arise via a gap junction with the ON–OFF DSGC (though we have not observed this feature in our connectomic reconstruction).…”

Section: Discussionmentioning

confidence: 72%

Origins of direction selectivity in the primate retina

et al. 2022

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From mouse to primate, there is a striking discontinuity in our current understanding of the neural coding of motion direction. In non-primate mammals, directionally selective cell types and circuits are a signature feature of the retina, situated at the earliest stage of the visual process. In primates, by contrast, direction selectivity is a hallmark of motion processing areas in visual cortex, but has not been found in the retina, despite significant effort. Here we combined functional recordings of light-evoked responses and connectomic reconstruction to identify diverse direction-selective cell types in the macaque monkey retina with distinctive physiological properties and synaptic motifs. This circuitry includes an ON-OFF ganglion cell type, a spiking, ON-OFF polyaxonal amacrine cell and the starburst amacrine cell, all of which show direction selectivity. Moreover, we discovered that macaque starburst cells possess a strong, non-GABAergic, antagonistic surround mediated by input from excitatory bipolar cells that is critical for the generation of radial motion sensitivity in these cells. Our findings open a door to investigation of a precortical circuitry that computes motion direction in the primate visual system.

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Section: Discussionmentioning

confidence: 72%

Origins of direction selectivity in the primate retina

et al. 2022

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“…The presence of direction selectivity in a spiking, polyaxonal, amacrine type linked to the recursive bistratified ganglion cell is distinctive, but parallels an emerging picture in the nonprimate mammal 11,63,79,80 . Direction selectivity in the ON-OFF A1 cell could arise via a gap junction with the ON-OFF DSGC (though we have not observed this feature in our 16 connectomic reconstruction).…”

Section: Discussionmentioning

confidence: 70%

“…Direction selectivity in the ON-OFF A1 cell could arise via a gap junction with the ON-OFF DSGC (though we have not observed this feature in our 16 connectomic reconstruction). If this were the case, the dominant axonal output synapse to bipolar-cell axon terminals could contribute to direction selectivity in the latter 80 .…”

Section: Discussionmentioning

confidence: 99%

Origins of direction selectivity in the primate retina

Kim

Peterson

Crook

et al. 2021

Preprint

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From mouse to primate, there is a striking discontinuity in our current understanding of the neural coding of motion direction. In non-primate mammals, directionally selective cell types and circuits are a signature feature of the retina, situated at the earliest stage of the visual process1,2. In primates, by contrast, direction selectivity is a hallmark of motion processing areas in visual cortex3,4, but has not been found in the retina, despite significant effort5,6. Here we combined functional recordings of light-evoked responses and connectomic reconstruction to identify diverse direction-selective cell types in the macaque monkey retina with distinctive physiological properties and synaptic motifs. This circuitry includes an ON-OFF ganglion cell type, a spiking, ON-OFF poly-axonal amacrine cell and the starburst amacrine cell, all of which show direction selectivity. Moreover, we found unexpectedly that macaque starburst cells possess a strong, non-GABAergic, antagonistic surround mediated by input from excitatory bipolar cells that is critical for the generation of radial motion sensitivity in these cells. Our findings open a new door to investigation of a novel circuitry that computes motion direction in the primate visual system.

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“…RSME visual stimulation module can be further used to vary the characteristics of the moving stimuli to dissect the set of mechanisms that enable a stable directional response. Fifth, while asymmetric inhibition is thought to be the key mechanism for DS, directionally-tuned excitation to DSGCs was also reported [28,51,52,[57][58][59]. RSME can be used to implement a directional excitatory input to the DSGC and test its contribution to the DSGC's directional preference.…”

Section: Discussionmentioning

confidence: 99%

Realistic retinal modeling unravels the differential role of excitation and inhibition to starburst amacrine cells in direction selectivity

et al. 2021

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Retinal direction-selectivity originates in starburst amacrine cells (SACs), which display a centrifugal preference, responding with greater depolarization to a stimulus expanding from soma to dendrites than to a collapsing stimulus. Various mechanisms were hypothesized to underlie SAC centrifugal preference, but dissociating them is experimentally challenging and the mechanisms remain debatable. To address this issue, we developed the Retinal Stimulation Modeling Environment (RSME), a multifaceted data-driven retinal model that encompasses detailed neuronal morphology and biophysical properties, retina-tailored connectivity scheme and visual input. Using a genetic algorithm, we demonstrated that spatiotemporally diverse excitatory inputs–sustained in the proximal and transient in the distal processes–are sufficient to generate experimentally validated centrifugal preference in a single SAC. Reversing these input kinetics did not produce any centrifugal-preferring SAC. We then explored the contribution of SAC-SAC inhibitory connections in establishing the centrifugal preference. SAC inhibitory network enhanced the centrifugal preference, but failed to generate it in its absence. Embedding a direction selective ganglion cell (DSGC) in a SAC network showed that the known SAC-DSGC asymmetric connectivity by itself produces direction selectivity. Still, this selectivity is sharpened in a centrifugal-preferring SAC network. Finally, we use RSME to demonstrate the contribution of SAC-SAC inhibitory connections in mediating direction selectivity and recapitulate recent experimental findings. Thus, using RSME, we obtained a mechanistic understanding of SACs’ centrifugal preference and its contribution to direction selectivity.

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Direction selectivity in retinal bipolar cell axon terminals

Cited by 34 publications

References 74 publications

Origins of direction selectivity in the primate retina

Origins of direction selectivity in the primate retina

Origins of direction selectivity in the primate retina

Realistic retinal modeling unravels the differential role of excitation and inhibition to starburst amacrine cells in direction selectivity

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