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

Gaynes, John A.; Budoff, Samuel A; Grybko, Michael J.; Hunt, Joshua B; Poleg-Polsky, Alon

doi:10.1038/s41467-022-32761-8

Cited by 20 publications

(33 citation statements)

References 95 publications

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“…In contrast, somatic recordings from starburst amacrines have often been made with radially moving stimuli, or stimuli masked near the soma (Euler et al, 2002; Hausselt et al, 2007; Oesch & Taylor, 2010; Fransen & Borghuis, 2017; Kim et al, 2022). Although such stimuli evoke strong somatic directional responses in starburst amacrines, recent studies provide evidence that this type of “appear-then-move” stimulus generates motion sensitivity in the presynaptic bipolar cells (Gaynes et al, 2022; Strauss et al, 2022). When this type of radial or masked stimulus first appears, it evokes a strong response to motion away from the bipolar RF center when the bipolar’s surround response is delayed.…”

Section: Methodsmentioning

confidence: 99%

“…The effect is especially evident in somatic recordings with radially moving stimuli centered over the starburst soma, because the radial stimulus evokes a strong motion sensitivity in proximal bipolar cells. However, stimuli that pass over the entire bipolar cell (and starburst) RF do not evoke this type of motion sensitivity because stimuli that pass into and out of the bipolar RF center evoke symmetric responses (Gaynes et al, 2022; Kim et al, 2022; Strauss et al, 2022). Therefore, for simplicity in the comparison between the morphological and space–time mechanisms, we chose to omit radial stimuli that would generate motion sensitivity originating in the bipolar cell from its center-surround RF.…”

Section: Methodsmentioning

confidence: 99%

“…Although such stimuli evoke strong somatic directional responses in starburst amacrines, recent studies provide evidence that this type of "appear-then-move" stimulus generates motion sensitivity in the presynaptic bipolar cells (Gaynes et al, 2022;Strauss et al, 2022). When this type of radial or masked stimulus first appears, it evokes a strong response to motion away from the bipolar RF center when the bipolar's surround response is delayed.…”

Section: Rationale For the Use Of Moving Bar Stimulimentioning

confidence: 99%

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Two mechanisms for direction selectivity in a model of the primate starburst amacrine cell

et al. 2023

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In a recent study, visual signals were recorded for the first time in starburst amacrine cells of the macaque retina, and, as for mouse and rabbit, a directional bias observed in calcium signals was recorded from near the dendritic tips. Stimulus motion from the soma toward the tip generated a larger calcium signal than motion from the tip toward the soma. Two mechanisms affecting the spatiotemporal summation of excitatory postsynaptic currents have been proposed to contribute to directional signaling at the dendritic tips of starbursts: (1) a “morphological” mechanism in which electrotonic propagation of excitatory synaptic currents along a dendrite sums bipolar cell inputs at the dendritic tip preferentially for stimulus motion in the centrifugal direction; (2) a “space–time” mechanism that relies on differences in the time-courses of proximal and distal bipolar cell inputs to favor centrifugal stimulus motion. To explore the contributions of these two mechanisms in the primate, we developed a realistic computational model based on connectomic reconstruction of a macaque starburst cell and the distribution of its synaptic inputs from sustained and transient bipolar cell types. Our model suggests that both mechanisms can initiate direction selectivity in starburst dendrites, but their contributions differ depending on the spatiotemporal properties of the stimulus. Specifically, the morphological mechanism dominates when small visual objects are moving at high velocities, and the space–time mechanism contributes most for large visual objects moving at low velocities.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Rationale For the Use Of Moving Bar Stimulimentioning

confidence: 99%

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Two mechanisms for direction selectivity in a model of the primate starburst amacrine cell

et al. 2023

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“…A second method utilized genetically encoded fluorescent glutamate sensors, such as iGluSnFR, to directly study the dynamics of BC release (Borghuis et al, 2013;Marvin et al, 2013). An examination of glutamate release dynamics confirmed the diverse signaling patterns within the lamina of the inner plexiform layer accessible to SAC dendrites (Franke et al, 2017;Gaynes et al, 2022;Strauss et al, 2022). Furthermore, excitatory drive to ON-DSGCs, which share many glutamatergic inputs with ON-SACs, was found to consist of units with distinct release dynamics, theoretically supporting the type of directional computation proposed by the space-time wiring hypothesis (Matsumoto et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…These protocols were specifically designed to target a small patch of retina beneath a single SAC dendrite or induce circularly-symmetric shrinking or expanding motion to elicit consistent responses across the dendritic tree (Euler et al, 2002;Hausselt et al, 2007;Koren et al, 2017;Oesch & Taylor, 2010). Nonlinear integration in BCs triggered by these visual stimuli may unintentionally introduce a directional bias to BC activation -contradicting the fundamental assumptions of the space-time wiring hypothesis (Gaynes et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Heterogeneous presynaptic receptive fields contribute to directional tuning in starburst amacrine cells

Gaynes

Budoff

Grybko

et al. 2023

Preprint

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The processing of visual information by retinal starburst amacrine cells (SACs) involves transforming excitatory input from bipolar cells (BCs) into directional calcium output. While previous studies have suggested that an asymmetry in the kinetic properties of bipolar cells along the soma-dendritic axes of the postsynaptic cell could enhance directional tuning at the level of individual branches, it remains unclear whether biologically relevant presynaptic kinetics contribute to direction selectivity when visual stimulation engages the entire dendritic tree. To address this question, we built multicompartmental models of the bipolar-SAC circuit and trained them to boost directional tuning. We report that despite significant dendritic crosstalk and dissimilar directional preferences along the dendrites that occur during whole-cell stimulation, the rules that guide BC kinetics leading to optimal directional selectivity are similar to the single-dendrite condition. To correlate model predictions to empirical findings, we utilized two-photon glutamate imaging to study the dynamics of bipolar release onto ON- and OFF-starburst dendrites in the murine retina. We reveal diverse presynaptic dynamics in response to motion in both BC populations; algorithms trained on the experimental data suggested that the differences in the temporal release kinetics are likely to correspond to heterogeneous receptive field (RF) properties among the different BC types, including the spatial extent of the center and surround components. In addition, we demonstrate that circuit architecture composed of presynaptic units with experimentally recorded dynamics could enhance directional drive but not to levels that replicate empirical findings, suggesting other DS mechanisms are required to explain SAC function. Our study provides new insights into the complex mechanisms underlying direction selectivity in retinal processing and highlights the potential contribution of presynaptic kinetics to the computation of visual information by starburst amacrine cells.

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Hierarchies in Visual Pathway: Functions and Inspired Artificial Vision

Zhu

Xie

et al. 2023

Advanced Materials

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The development of artificial intelligence has posed a challenge to machine vision based on conventional complementary metal‐oxide semiconductor (CMOS) circuits owing to its high latency and inefficient power consumption originating from the data shuffling between memory and computation units. Gaining more insight into the function of every part of the visual pathway for visual perception could bring the capabilities of machine vision in terms of robustness and generality. Hardware acceleration of more energy efficient and biorealistic artificial vision highly necessitates neuromorphic devices and circuits which are able to mimic the function of each part of visual pathway. In this paper, we review the structure and function of the entire class of visual neurons from retina to the primate visual cortex within reach (chapter 2). Based on the extraction of biological principles, the recent hardware implemented visual neurons located in different parts of the visual pathway are detailed discussed (chapter 3 and chapter 4). Furthermore, we attempt to provide valuable applications of inspired artificial vision in different scenarios (chapter 5). The functional description of the visual pathway and its inspired neuromorphic devices/circuits are expected to provide valuable insights for the design of next‐generation artificial visual perception systems.This article is protected by copyright. All rights reserved

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

Cited by 20 publications

References 95 publications

Two mechanisms for direction selectivity in a model of the primate starburst amacrine cell

Two mechanisms for direction selectivity in a model of the primate starburst amacrine cell

Heterogeneous presynaptic receptive fields contribute to directional tuning in starburst amacrine cells

Hierarchies in Visual Pathway: Functions and Inspired Artificial Vision

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