Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

Ding, Jennifer; Chen, Albert; Chung, Joaquín; Ledesma, Héctor Acarón; Wu, Mofei; Berson, David M.; Palmer, Stéphanie; Wei, Wei

doi:10.7554/elife.68181

Cited by 5 publications

(5 citation statements)

References 70 publications

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“…5 A , B ; Table 4 ). This is consistent with recent reports investigating another nDSGC subtype, where the glutamatergic receptive field was also skewed toward the DSGC’s null direction ( Ding et al, 2021 ). Additionally, although glutamatergic receptive field were significantly larger than dendritic field size ( Fig.…”

Section: Resultssupporting

confidence: 93%

“…Here, we find that the while the glutamatergic receptive fields of nDSGCs are skewed toward the DSGC’s null direction, consistent with previous reports ( Ding et al, 2021 ), the glutamatergic receptive fields of vDSGCs are skewed toward their preferred side. However, vDSGCs were previously reported to exhibit lag normalized synaptic responses because of gap junction coupling, enabling them to encode object location ( Trenholm et al, 2013 ).…”

Section: Discussionsupporting

confidence: 93%

“…In contrast, the orientation of the glutamate receptive field in nDSGCs was not oriented toward its preferred direction but rather, on average, was oriented towards the DSGCs' null direction (180˚) (mean ± SD ON= 200 ± 68˚; OFF= 220± 72˚, n=10) (Figures 5A and B) (Table 4). This is consistent with recent reports investigating another nDSGC subtype, where the glutamatergic receptive field was also skewed towards the DSGC's null direction (Ding et al, 2021). Additionally, though glutamatergic receptive field were significantly larger than dendritic field size (Figure 5C), they were closer in area than mixed glutamatergiccholinergic receptive field size (compare Figure 5C with 5D, left), indicating that cholinergic inputs from SACs contribute excitatory inputs outside of the DSGC dendrites.…”

Section: Dsgc Dendritic Morphology Does Determine the Organization Of Spatial Receptive Fieldssupporting

confidence: 91%

“…However, receptive field mapping informs us of the overall synaptic distribution onto DSGC dendrites that could be activated by a variety of different visual stimuli. For example, a recent study has also implicated variations in the strength of excitatory receptive field, along the null-preferred axis, is critical for the ability to encode the location of moving stimuli and is revealed when the motion stimulus is interrupted by stationary occluder ( Ding et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…This is the classical mechanism postulated to underlie direction-selective responses in both the retina (Fried et al, 2002;Yonehara et al, 2011) and in the visual cortex (Hubel & Wiesel, 1959, 1962Priebe & Ferster, 2005;Rossi et al, 2020). Several studies have revealed temporal delays, consistent with spatially offset inhibition, play a role in the DS computation of the mouse retina (Hanson et al, 2019;Pei et al, 2015;Ding et al, 2021). Recently, we used receptive field mapping to show that a population of asymmetric, ventral preferring DSGCs (vDSGCs) have both tuned inhibitory inputs and spatially offset inhibition, though neither of these circuit contributions were impacted by dramatic changes in the dendrite orientation due to dark-rearing (El-Quessny et al, 2020).…”

Section: Introductionmentioning

confidence: 93%

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Dendrite Morphology Minimally Influences the Synaptic Distribution of Excitation and Inhibition in Retinal Direction-Selective Ganglion Cells

El-Quessny

Feller

2021

eNeuro

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Throughout the nervous system, the organization of excitatory and inhibitory synaptic inputs within a neuron’s receptive field shapes its output computation. In some cases, multiple motifs of synaptic organization can contribute to a single computation. Here, we compare two of these mechanisms performed by two morphologically distinct retinal direction-selective ganglion cells (DSGCs): directionally tuned inhibition and spatially offset inhibition. Using drifting stimuli, we found that DSGCs that have asymmetric dendrites exhibited stronger directionally tuned inhibition than symmetric DSGCs. Using stationary stimuli to map receptive fields, we found that DSGCs with both symmetric and asymmetric dendrites exhibited similar spatially offset inhibition. Interestingly, we observed that excitatory and inhibitory synapses for both cell types were locally correlated in strength. This result indicates that in the mouse retina, dendritic morphology influences the amount of tuned inhibition attained through asymmetric wiring but does not dictate the synaptic organization of excitation relative to inhibition.

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Section: Resultssupporting

confidence: 93%

Section: Discussionsupporting

confidence: 93%

Section: Dsgc Dendritic Morphology Does Determine the Organization Of Spatial Receptive Fieldssupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 93%

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Dendrite Morphology Minimally Influences the Synaptic Distribution of Excitation and Inhibition in Retinal Direction-Selective Ganglion Cells

El-Quessny

Feller

2021

eNeuro

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Classical center-surround receptive fields facilitate novel object detection in retinal bipolar cells

et al. 2022

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Antagonistic interactions between center and surround receptive field (RF) components lie at the heart of the computations performed in the visual system. Circularly symmetric center-surround RFs are thought to enhance responses to spatial contrasts (i.e., edges), but how visual edges affect motion processing is unclear. Here, we addressed this question in retinal bipolar cells, the first visual neuron with classic center-surround interactions. We found that bipolar glutamate release emphasizes objects that emerge in the RF; their responses to continuous motion are smaller, slower, and cannot be predicted by signals elicited by stationary stimuli. In our hands, the alteration in signal dynamics induced by novel objects was more pronounced than edge enhancement and could be explained by priming of RF surround during continuous motion. These findings echo the salience of human visual perception and demonstrate an unappreciated capacity of the center-surround architecture to facilitate novel object detection and dynamic signal representation.

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A new role for excitation in the retinal direction‐selective circuit

Ankri,

Riccitelli,

Rivlin‐Etzion

2024

The Journal of Physiology

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A key feature of the receptive field of neurons in the visual system is their centre–surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more complex processing remains poorly understood. Here, we investigate the role of centre and surround receptive fields in retinal direction selectivity by exposing posterior‐preferring On–Off direction‐selective ganglion cells (pDSGCs) to adaptive light and recording their response to globally moving objects. We reveal that light adaptation leads to surround expansion in pDSGCs. The pDSGCs maintain their original directional tuning in the centre receptive field, but present the oppositely tuned response in their surround. Notably, although inhibition is the main substrate for retinal direction selectivity, we found that following light adaptation, both the centre‐ and surround‐mediated responses originate from directionally tuned excitatory inputs. Multi‐electrode array recordings show similar oppositely tuned responses in other DSGC subtypes. Together, these data attribute a new role for excitation in the direction‐selective circuit. This excitation carries an antagonistic centre–surround property, possibly designed to sharpen the detection of motion direction in the retina. imageKey points Receptive fields of direction‐selective retinal ganglion cells expand asymmetrically following light adaptation. The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation. Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction. GABAergic and glycinergic inputs modulate the null‐tuned delayed response differentially. Null‐tuned delayed spiking phases can be detected in all types of direction‐selective retinal ganglion cells. Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.

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Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

Cited by 5 publications

References 70 publications

Dendrite Morphology Minimally Influences the Synaptic Distribution of Excitation and Inhibition in Retinal Direction-Selective Ganglion Cells

Dendrite Morphology Minimally Influences the Synaptic Distribution of Excitation and Inhibition in Retinal Direction-Selective Ganglion Cells

Classical center-surround receptive fields facilitate novel object detection in retinal bipolar cells

A new role for excitation in the retinal direction‐selective circuit

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