Synaptic Rectification Controls Nonlinear Spatial Integration of Natural Visual Inputs

Turner, Maxwell H.; Rieke, Fred

doi:10.1016/j.neuron.2016.05.006

Cited by 90 publications

(172 citation statements)

References 51 publications

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“…RGC firing rates showed a modulation for both white noise and the null stimulus that was highly reproducible across repeats ( Figure 6C, D), indicating that the visual inputs are not integrated linearly across the RF. Note that the null stimulus modulated OFF parasol cells more strongly than ON parasol cells, consistent with previous results obtained with white noise and natural scene stimuli (Chichilnisky & Kalmar 2002, Demb et al, 2001, Turner & Rieke 2016; henceforth, analysis is focused on OFF parasol cells.…”

Section: Subunit Model Explains Spatial Nonlinearities Revealed By Nusupporting

confidence: 87%

Inference of Nonlinear Spatial Subunits in Primate Retina with Spike-Triggered Clustering

Shah

Brackbill

Rhoades

et al. 2018

Preprint

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AbstractIntegration of rectified synaptic inputs is a widespread nonlinear motif in sensory neuroscience. We present a novel method for maximum likelihood estimation of nonlinear subunits by soft-clustering spike-triggered stimuli. Subunits estimated from parasol ganglion cells recorded in macaque retina partitioned the receptive field into compact regions, likely representing bipolar cell inputs. Joint clustering with multiple RGCs revealed shared subunits in neighboring cells, producing a parsimonious population model. Closed-loop subunit validation was then performed by projecting white noise into the null space of the linear receptive field. Responses to these null stimuli were more accurately explained by a model with multiple subunits, and were stronger in OFF cells than ON cells. Presentation of natural stimuli containing jittering edges and textures also revealed greater response prediction accuracy with the subunit model. Finally, the generality of the approach was demonstrated by application to V1 data.

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Section: Subunit Model Explains Spatial Nonlinearities Revealed By Nusupporting

confidence: 87%

Inference of Nonlinear Spatial Subunits in Primate Retina with Spike-Triggered Clustering

Shah

Brackbill

Rhoades

et al. 2018

Preprint

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“…Consistent with this hypothesis, direction selectivity of the On response of DSGCs in Gabra2 KO mice is normal when the background is homogeneous but deteriorates as soon as white noise is introduced into the background. These findings represent an intriguing example in which additional neural mechanisms are recruited when the visual stimulus more closely resembles natural viewing conditions, but simpler visual stimuli involving only the feature of interest may not reveal the functional significance of these mechanisms (David et al, 2004; Felsen and Dan, 2005; Felsen et al, 2005; Turner and Rieke, 2016). A notable analogy has been reported in the visual cortex: a prominent inhibitory component in the receptive field of visual cortical neurons is uniquely revealed by more complex natural stimuli but is not observed with synthetic sinusoidal gratings (David et al, 2004).…”

Section: Discussionmentioning

confidence: 95%

Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity

Chen

Pei

Koren

et al. 2016

eLife

104

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The dendrites of starburst amacrine cells (SACs) in the mammalian retina are preferentially activated by motion in the centrifugal direction, a property that is important for generating direction selectivity in direction selective ganglion cells (DSGCs). A candidate mechanism underlying the centrifugal direction selectivity of SAC dendrites is synaptic inhibition onto SACs. Here we disrupted this inhibition by perturbing distinct sets of GABAergic inputs onto SACs – removing either GABA release or GABA receptors from SACs. We found that lateral inhibition onto Off SACs from non-SAC amacrine cells is required for optimal direction selectivity of the Off pathway. In contrast, lateral inhibition onto On SACs is not necessary for direction selectivity of the On pathway when the moving object is on a homogenous background, but is required when the background is noisy. These results demonstrate that distinct sets of inhibitory mechanisms are recruited to generate direction selectivity under different visual conditions.DOI: http://dx.doi.org/10.7554/eLife.21053.001

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“…Tissue sensitivity was assessed at the beginning of each experiment by ensuring ON parasol RGCs responded to a full-field, 5% contrast, 4 Hz temporally-modulated spot. 74 ON parasol RGCs lack significant S-cone input and were also used to validate the S-cone isolating stimuli. 32 For each subsequent RGC encountered, the polarity (ON, OFF or ON-OFF) and cell type were first determined by spots presenting high contrast luminance increments and decrements from a photopic mean light level.…”

Section: Recording Protocolmentioning

confidence: 99%

An S-cone circuit for edge detection in the primate retina

Patterson

Kuchenbecker

Anderson

et al. 2019

Preprint

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Midget retinal ganglion cells (RGCs) are the most common RGC type in the primate retina. Their responses mediate both color and spatial vision, yet the specific links between midget RGC responses and visual perception are unclear. Previous research on the dual roles of midget RGCs has focused on those comparing long (L) vs. middle (M) wavelength sensitive cones. However, there is evidence for several other rare midget RGC subtypes receiving S-cone input, but their role in color and spatial vision is uncertain. Here, we confirm the existence of the single S-cone center OFF midget RGC circuit in the central retina of macaque monkey both structurally and functionally, by combining single cell electrophysiology with 3D electron microscopy reconstructions of the upstream circuitry. Like the well-studied L vs. M midget RGCs, the S-OFF midget RGCs have a centersurround receptive field consistent with a role in spatial vision. While spectral opponency in a primate RGC is classically assumed to contribute to hue perception, a role supporting edge detection is more consistent with the S-OFF midget RGC receptive field structure and studies of hue perception.

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Synaptic Rectification Controls Nonlinear Spatial Integration of Natural Visual Inputs

Cited by 90 publications

References 51 publications

Inference of Nonlinear Spatial Subunits in Primate Retina with Spike-Triggered Clustering

Inference of Nonlinear Spatial Subunits in Primate Retina with Spike-Triggered Clustering

Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity

An S-cone circuit for edge detection in the primate retina

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