Dataset Information

Special nuclear layer contacts between starburst amacrine cells in the mouse retina.

ABSTRACT: Starburst amacrine cells are a prominent neuron type in the mammalian retina that has been well-studied for its role in direction-selective information processing. One specific property of these cells is that their dendrites tightly stratify at specific depths within the inner plexiform layer (IPL), which, together with their unique expression of choline acetyltransferase (ChAT), has made them the most common depth marker for studying other retinal neurons in the IPL. This stratifying property makes it unexpected that they could routinely have dendrites reaching into the nuclear layer or that they could have somatic contact specializations, which is exactly what we have found in this study. Specifically, an electron microscopic image volume of sufficient size from a mouse retina provided us with the opportunity to anatomically observe both microscopic details and collective patterns, and our detailed cell reconstructions revealed interesting cell-cell contacts between starburst amacrine neurons. The contact characteristics differ between the respective On and Off starburst amacrine subpopulations, but both occur within the soma layers, as opposed to their regular contact laminae within the inner plexiform layer.

SUBMITTER: Mu S

PROVIDER: S-EPMC11182129 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Special nuclear layer contacts between starburst amacrine cells in the mouse retina.

Mu Shang S Turner Nicholas L NL Silversmith William M WM Jordan Chris S CS Kemnitz Nico N Sorek Marissa M David Celia C Jones Devon L DL Bland Doug D Moore Merlin M Sterling Amy Robinson AR Seung H Sebastian HS

Frontiers in ophthalmology 20230324

Starburst amacrine cells are a prominent neuron type in the mammalian retina that has been well-studied for its role in direction-selective information processing. One specific property of these cells is that their dendrites tightly stratify at specific depths within the inner plexiform layer (IPL), which, together with their unique expression of choline acetyltransferase (ChAT), has made them the most common depth marker for studying other retinal neurons in the IPL. This stratifying property m ...[more]

PMID: 38983098

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Project description:BackgroundDeveloping retinas display retinal waves, the patterned spontaneous activity essential for circuit refinement. During the first postnatal week in rodents, retinal waves are mediated by synaptic transmission between starburst amacrine cells (SACs) and retinal ganglion cells (RGCs). The neuromodulator adenosine is essential for the generation of retinal waves. However, the cellular basis underlying adenosine's regulation of retinal waves remains elusive. Here, we investigated whether and how the adenosine A(2A) receptor (A(2A)R) regulates retinal waves and whether A(2A)R regulation of retinal waves acts via presynaptic SACs.Methodology/principal findingsWe showed that A(2A)R was expressed in the inner plexiform layer and ganglion cell layer of the developing rat retina. Knockdown of A(2A)R decreased the frequency of spontaneous Ca²⁺ transients, suggesting that endogenous A(2A)R may up-regulate wave frequency. To investigate whether A(2A)R acts via presynaptic SACs, we targeted gene expression to SACs by the metabotropic glutamate receptor type II promoter. Ca²⁺ transient frequency was increased by expressing wild-type A(2A)R (A2AR-WT) in SACs, suggesting that A(2A)R may up-regulate retinal waves via presynaptic SACs. Subsequent patch-clamp recordings on RGCs revealed that presynaptic A(2A)R-WT increased the frequency of wave-associated postsynaptic currents (PSCs) or depolarizations compared to the control, without changing the RGC's excitability, membrane potentials, or PSC charge. These findings suggest that presynaptic A(2A)R may not affect the membrane properties of postsynaptic RGCs. In contrast, by expressing the C-terminal truncated A(2A)R mutant (A(2A)R-ΔC) in SACs, the wave frequency was reduced compared to the A(2A)R-WT, but was similar to the control, suggesting that the full-length A(2A)R in SACs is required for A(2A)R up-regulation of retinal waves.Conclusions/significanceA(2A)R up-regulates the frequency of retinal waves via presynaptic SACs, requiring its full-length protein structure. Thus, by coupling with the downstream intracellular signaling, A(2A)R may have a great capacity to modulate patterned spontaneous activity during neural circuit refinement.

Project description: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 BCs 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 (DS) 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 DS 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 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 DS in retinal processing and highlights the potential contribution of presynaptic kinetics to the computation of visual information by SACs.

Project description: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.

Dataset Information

Special nuclear layer contacts between starburst amacrine cells in the mouse retina.

Publications

Special nuclear layer contacts between starburst amacrine cells in the mouse retina.

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