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

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 comple...

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Veröffentlicht in:The Journal of physiology 2024-11, Vol.602 (22), p.6301-6328
Hauptverfasser: Ankri, Lea, Riccitelli, Serena, Rivlin‐Etzion, Michal
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Rivlin‐Etzion, Michal
description 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. Key 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. figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation stre
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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. Key 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. figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation strengthened the On response at the expense of the Off response. Moreover, it exposed a delayed spiking phase, which is tuned to the ND. Intracellular recordings revealed that before light adaptation, inhibition rules the directional response, whereas after light adaptation, both early and delayed directional responses are dominated by excitation. 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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. Key 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. figure legend Direction‐selective retinal ganglion cells (DSGCs) respond to motion in the ‘preferred direction’ (PD), but barely to the motion in the opposite, ‘null direction’ (ND). Using targeted patch‐clamp and multi‐electrode array recordings, we investigated the effects of light adaptation on the response of DSGCs to moving bars. Light adaptation strengthened the On response at the expense of the Off response. Moreover, it exposed a delayed spiking phase, which is tuned to the ND. Intracellular recordings revealed that before light adaptation, inhibition rules the directional response, whereas after light adaptation, both early and delayed directional responses are dominated by excitation. 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subjects Acuity
Adaptation
Adaptation, Ocular - physiology
Animals
centre–surround
Delayed response
direction selectivity
electrophysiology
Information processing
Light
light adaptation
Motion Perception - physiology
mouse retina
multi‐electrode array
Photic Stimulation - methods
Receptive field
Retina
Retina - physiology
retinal ganglion cell
Retinal ganglion cells
Retinal Ganglion Cells - physiology
Visual system
γ-Aminobutyric acid
title A new role for excitation in the retinal direction‐selective circuit
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