Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina

Ankri, Lea; Tsur, Elishai Ezra; Maimon, Shir R.; Kaushansky, Nathali; Rivlin‐Etzion, Michal

doi:10.1016/j.celrep.2020.107608

Cited by 28 publications

(34 citation statements)

References 44 publications

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“…Passive models predict weak CF preference in SAC distal dendrites and a CP preference in the soma [19]. In our simulation, the precise excitatory inputs found by the genetic algorithm were enough to trigger a CF preference in the passive SAC soma, in accordance with experimental results [9,15,22,32]. In response to the circular rings, we found that the somatic and dendritic voltage closely match, in line with a previous study [15].…”

Section: Discussionsupporting

confidence: 91%

“…We previously demonstrated SAC CF preference using patch-clamp recordings from On-SACs in the isolated mouse retina [ 32 ]. The electrophysiological SAC recordings presented here combine published and new data.…”

Section: Resultsmentioning

confidence: 99%

“…Using RSME, we were able to dissect the network mechanisms, which rely on the PLOS COMPUTATIONAL BIOLOGY architecture of SAC excitatory and inhibitory inputs. In the mouse retina, excitatory inputs from bipolar cells to SAC are concentrated in the 2/3 proximal parts of its processes [10,11,32]. The genetic algorithm identified CF-preferring SACs with a matched input distribution, but it also demonstrated that CF preference could arise when the excitatory inputs are confined to an even smaller area around the cell soma.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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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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“…A decrease in On-Off DSGC dendritic field size from the dorsal to the ventral retina has been reported 45 . Moreover, On starburst amacrine cells in the dorsal retina can reverse their contrast polarity under certain visual stimulation conditions, a phenomenon that likely originates from region-specific photoreceptor properties and may contribute to the switch of the DSGC directional preference 36,37,46 .…”

Section: Discussionmentioning

confidence: 99%

Visual stimulation induces distinct forms of sensitization of On-Off direction-selective ganglion cell responses in the dorsal and ventral retina

Xue-song

et al. 2021

Preprint

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Experience-dependent modulation of neuronal responses is a key attribute in sensory processing. In the mammalian retina, the On-Off direction-selective ganglion cell (On-Off DSGC) is well known for its robust direction selectivity. However, how the On-Off DSGC light responsiveness dynamically adjusts to the changing visual environment is underexplored. Here, we report that the On-Off DSGC can be transiently sensitized by prior stimuli. Notably, distinct sensitization patterns are found in dorsal and ventral DSGCs that receive visual inputs from lower and upper visual fields respectively. Although responses of both dorsal and ventral DSGCs to dark stimuli (Off responses) are sensitized, only dorsal cells show sensitization of responses to bright stimuli (On responses). Visual stimulation to the dorsal retina potentiates a sustained excitatory input from Off bipolar cells, leading to tonic depolarization of dorsal DSGCs. Such tonic depolarization propagates from the Off to the On dendritic arbor of the DSGC to sensitize its On response. We also identified a previously overlooked feature of DSGC dendritic architecture that can support direct electrotonic propagation between On and Off dendritic layers. By contrast, ventral DSGCs lack a sensitized tonic depolarization and thus do not exhibit sensitization of their On responses. Our results highlight a topographic difference in Off bipolar cell inputs underlying divergent sensitization patterns of dorsal and ventral On-Off DSGCs. Moreover, substantial crossovers between dendritic layers of On-Off DSGCs suggest an interactive dendritic algorithm for processing On and Off signals before they reach the soma.

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“…One possible modeling for J would be J = α xJ bias , where α is a gain term and J bias is a fixed background current. Neurons often have some preferred stimuli e (preferred direction, or encoder) to which they respond with a high frequency of spikes [e.g., direction selectivity in retinal ganglion cells ( Ankri et al, 2020 )]. J will therefore be more appropriately defined using: J = α x ⋅ eJ bias , where x ⋅ e equals 1 when both x and e are in the same direction, and 0 when they are opposing each other.…”

Section: Methodsmentioning

confidence: 99%

Neuromorphic Analog Implementation of Neural Engineering Framework-Inspired Spiking Neuron for High-Dimensional Representation

Hazan

Tsur

2021

Front. Neurosci.

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Brain-inspired hardware designs realize neural principles in electronics to provide high-performing, energy-efficient frameworks for artificial intelligence. The Neural Engineering Framework (NEF) brings forth a theoretical framework for representing high-dimensional mathematical constructs with spiking neurons to implement functional large-scale neural networks. Here, we present OZ, a programable analog implementation of NEF-inspired spiking neurons. OZ neurons can be dynamically programmed to feature varying high-dimensional response curves with positive and negative encoders for a neuromorphic distributed representation of normalized input data. Our hardware design demonstrates full correspondence with NEF across firing rates, encoding vectors, and intercepts. OZ neurons can be independently configured in real-time to allow efficient spanning of a representation space, thus using fewer neurons and therefore less power for neuromorphic data representation.

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Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina

Cited by 28 publications

References 44 publications

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

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

Visual stimulation induces distinct forms of sensitization of On-Off direction-selective ganglion cell responses in the dorsal and ventral retina

Neuromorphic Analog Implementation of Neural Engineering Framework-Inspired Spiking Neuron for High-Dimensional Representation

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