Spatiotemporally Asymmetric Excitation Supports Mammalian Retinal Motion Sensitivity

Matsumoto, Akira; Briggman, Kevin L.; Yonehara, Keisuke

doi:10.1016/j.cub.2019.08.048

Cited by 55 publications

(100 citation statements)

References 55 publications

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“…Furthermore, a recent analysis of subcellular glutamate transients in ON DSGC dendrites suggests that the glutamatergic excitatory input comes from kinetically distinct bipolar cell types (Matsumoto et al, 2019). Here, optimal temporal summation during preferred motion occurs over the course of the DSGC's entire dendritic arbor.…”

Section: Implications For Local Dendritic Integrationmentioning

confidence: 99%

The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

Jain

Murphy-Baum

deRosenroll

et al. 2019

Preprint

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2 SUMMARYRecent studies indicate that the precise timing and location of excitation and inhibition (E/I) within active dendritic trees can significantly impact neuronal function. How excitatory and inhibitory inputs are functionally organized at the subcellular level in intact circuits remains unclear. To address this issue, we took advantage of the retinal direction-selective ganglion cell circuit, in which directionally tuned inhibitory GABAergic input arising from starburst amacrine cells shape direction-selective dendritic responses. We combined two-photon Ca 2+ imaging with genetic, pharmacological, and single-cell ablation methods to examine local E/I. We demonstrate that when active dendritic conductances are blocked, direction selectivity emerges semiindependently within unusually small dendritic segments (<10 µm). Impressively, the direction encoded by each segment is relatively homogenous throughout the ganglion cell's dendritic tree.Together the results demonstrate a precise subcellular functional organization of excitatory and inhibitory input, which suggests that the parallel processing scheme proposed for direction encoding could be more fine-grained than previously envisioned. 3 3

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Section: Implications For Local Dendritic Integrationmentioning

confidence: 99%

The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

Jain

Murphy-Baum

deRosenroll

et al. 2019

Preprint

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“…One possibility is that bipolar cell inputs on the preferred side are stronger and therefore dendrites on the preferred side are stabilized while dendrites on the non-preferred side are pruned. Such asymmetric wiring of bipolar cells was recently reported in ON DSGCs (Matsumoto et al, 2019). However, serial EM reconstructions of symmetric ON-OFF DSGCs (Ding et al, 2016) do not indicate such a bias, though this reconstruction has not been conducted for vDSGCs.…”

Section: Activity Influences Dendritic Morphologymentioning

confidence: 76%

“…Whether visual experience is critical for the maturation of the source of nonlinear postsynaptic conductance, e.g. voltage gated conductances or electrical coupling, or the organization and kinetics of excitatory inputs onto DSGC dendrites (Matsumoto et al, 2019) remains to be determined.…”

Section: Implications For Postsynaptic Contributions To Dsmentioning

confidence: 99%

Visual experience instructs dendrite orientation but is not required for asymmetric wiring of the retinal direction selective circuit

El-Quessny

Maanum

Feller

2019

Preprint

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Changes in dendritic morphology in response to activity have long been thought to be a critical component of how neural circuits develop to properly encode sensory information. Here we report the impact of dark-rearing on the dendritic morphology and function of a retinal ganglion cell type, a ventral-preferring direction-selective ganglion cell (vDSGC). vDSGCs have asymmetric dendrites oriented along their preferred direction. We found that, at eye opening, vDSGC dendrites are not yet ventrally oriented, and that, surprisingly, dark-rearing prevents ventral orientation of vDSGC dendrites. Despite their dramatic change in dendritic morphology, vDSGCs in dark-reared mice maintain ventral directional preference. Direction selective tuning in dark-reared mice is mediated by asymmetric inhibition, as observed in vDSGCs of normally reared animals. Hence, we postulate that dendritic form follows proper circuit function, where dendritic orientation is refined over the course of development and is dependent on structured visual experience following eye opening.

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“…Here, we modeled the BC5 subtype that expresses voltage-gated sodium channels 29 which probably also corresponds to the more transient BC5 subtype reported in 30 . The TTX sensitivity observed in 31 suggests that both, 5o and 5i express voltage-gated sodium channels. To make our model consistent, we used data from the same BC5 subtype (5o) for the morphology, the target data and the number of cone contacts.…”

Section: Ion Channels and Synapses -Literature Reviewmentioning

confidence: 99%

Bayesian inference for biophysical neuron models enables stimulus optimization for retinal neuroprosthetics

Oesterle

Behrens

Schroeder

et al. 2020

Preprint

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Multicompartment models have long been used to study the biophysical mechanisms underlying neural information processing. However, it has been challenging to infer the parameters of such models from data. Here, we build on recent advances in Bayesian simulation-based inference to estimate the parameters of detailed models of retinal neurons whose anatomical structure was based on electron microscopy data. We demonstrate how parameters of a cone, an OFF-and an ON-cone bipolar cell model can be inferred from standard two-photon glutamate imaging with simple light stimuli. The inference method starts with a prior distribution informed by literature knowledge and yields a posterior distribution over parameters highlighting parameters consistent with the data. This posterior allows determining how well parameters are constrained by the data and to what extent changes in one parameter can be compensated for by changes in another. To demonstrate the potential of such data-driven mechanistic neuron models, we created a simulation environment for external electrical stimulation of the retina as used in retinal neuroprosthetic devices. We used the framework to optimize the stimulus waveform to selectively target OFFand ON-cone bipolar cells, a current major problem of retinal neuroprothetics. Taken together, this study demonstrates how a data-driven Bayesian simulation-based inference approach can be used to estimate parameters of complex mechanistic models with high-throughput imaging data.Constraining many of these model parameters such as channel densities requires highly specialized and technically challenging experiments, and, hence, it is usually not viable to measure every single parameter for a neuron model of a specific neuron type. Rather, parameters for mechanistic simulations are often aggregated over different neuron types and even across species. Even though this may be justified in specific cases it likely limits our ability to identify mechanistic models of individual cell types. Alternatively, parameter search methods have been proposed to identify the parameters of mechanistic neuron models from standardized patch-clamp protocols based on exhaustive grid-searches 9-11 or evolutionary algorithms [12][13][14][15] . Such methods are often inefficient, typically not applicable for models with many parameters and identify only a single point estimate consistent with the data instead of the entire distribution.Here, we built on recent advances in Bayesian simulation-based inference to fit multicompartment models of neurons with realistic anatomy in the mouse retina. We used a framework called Sequential Neural Posterior Estimation (SNPE) 16,17 to identify model parameters based on high-throughput two-photon measurements of these neurons' responses to light stimuli. SNPE is a Bayesian simulation-based inference algorithm that allows parameter estimation for simulator models for which the likelihood cannot be evaluated easily. The algorithm estimates the distribution of model parameters consistent with specified ...

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Spatiotemporally Asymmetric Excitation Supports Mammalian Retinal Motion Sensitivity

Cited by 55 publications

References 55 publications

The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

Visual experience instructs dendrite orientation but is not required for asymmetric wiring of the retinal direction selective circuit

Bayesian inference for biophysical neuron models enables stimulus optimization for retinal neuroprosthetics

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