Direction selectivity

Murphy-Baum, Benjamin L.; Schwartz, Gregory William; Awatramani, Gautam B.

doi:10.1016/b978-0-12-819896-4.00012-3

Cited by 4 publications

(1 citation statement)

References 104 publications

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“…Starburst amacrine cells (SACs) release acetylcholine and GABA onto neighboring cells ( O’Malley et al, 1992 ) and play an important role in the formation of direction selectivity in the adult retina ( Yoshida et al, 2001 ; Amthor et al, 2002 ). To elucidate the mechanisms underlying direction selectivity, many researchers focused on neural computation mechanisms on the dendrites of SACs ( Wei, 2018 ; Murphy-Baum et al, 2021 ), such as the distribution of channels ( Ozaita et al, 2004 ; Gavrikov et al, 2006 ) and centrifugal signal transmission along dendrites ( Euler et al, 2002 ; Lee and Zhou, 2006 ; Hausselt et al, 2007 ), as well as input-output relationships between SACs ( Lee and Zhou, 2006 ), SACs and direction-selective ganglion cells ( Lee et al, 2010 ; Briggman et al, 2011 ), SACs and bipolar cells ( Kim et al, 2014 ; Ding et al, 2016 ), and SACs and other amacrine cells ( Jain et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Starburst amacrine cells form gap junctions in the early postnatal stage of the mouse retina

Maruyama

Ishii

Kaneda

2023

Front. Cell. Neurosci.

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Although gap junctional coupling in the developing retina is important for the maturation of neuronal networks, its role in the development of individual neurons remains unclear. Therefore, we herein investigated whether gap junctional coupling by starburst amacrine cells (SACs), a key neuron for the formation of direction selectivity, occurs during the developmental stage in the mouse retina. Neurobiotin-injected SACs coupled with many neighboring cells before eye-opening. The majority of tracer-coupled cells were retinal ganglion cells, and tracer coupling was not detected between SACs. The number of tracer-coupled cells significantly decreased after eye-opening and mostly disappeared by postnatal day 28 (P28). Membrane capacitance (Cm), an indicator of the formation of electrical coupling with gap junctions, was larger in SACs before than after eye-opening. The application of meclofenamic acid, a gap junction blocker, reduced the Cm of SACs. Gap junctional coupling by SACs was regulated by dopamine D1 receptors before eye-opening. In contrast, the reduction in gap junctional coupling after eye-opening was not affected by visual experience. At the mRNA level, 4 subtypes of connexins (23, 36, 43, and 45) were detected in SACs before eye-opening. Connexin 43 expression levels significantly decreased after eye-opening. These results indicate that gap junctional coupling by SACs occurs during the developmental period and suggest that the elimination of gap junctions proceeds with the innate system.

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Section: Introductionmentioning

confidence: 99%

Starburst amacrine cells form gap junctions in the early postnatal stage of the mouse retina

Maruyama

Ishii

Kaneda

2023

Front. Cell. Neurosci.

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Spatiotemporal properties of glutamate input support direction selectivity in the dendrites of retinal starburst amacrine cells

Srivastava

deRosenroll

Murphy-Baum

et al. 2022

Preprint

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The asymmetric summation of kinetically distinct glutamate inputs across the dendrites of retinal “starburst” amacrine cells is proposed to underlie their direction selective properties, but experimentally verifying input kinetics has been challenging. Here, we used two-photon glutamate sensor (iGluSnFR) imaging to directly measure the input kinetics across individual starburst dendrites. We found that signals measured from proximal dendrites were relatively sustained compared to those measured from distal dendrites. These differences were observed across a range of stimulus sizes and appeared to be shaped mainly by excitatory rather than inhibitory network interactions. Temporal deconvolution analysis suggests that the steady-state vesicle release rate was ~ 3 times larger at proximal sites compared to distal sites. Using a connectomics-inspired computational model, we demonstrate that input kinetics play an important role in shaping direction selectivity at low stimulus velocities. Together, these results provide direct support for the ‘space-time wiring’ model for direction selectivity.

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Neural Circuits Underlying Multifeature Extraction in the Retina

Chander,

Hanson,

Chundekkad

et al. 2023

J. Neurosci.

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Classic ON-OFF direction-selective ganglion cells (DSGCs) that encode the four cardinal directions were recently shown to also be orientation-selective. To clarify the mechanisms underlying orientation selectivity we employed a variety of electrophysiological, optogenetic, and gene knock-out strategies to test the relative contributions of glutamate, GABA, and acetylcholine (ACh) input that are known to drive DSGCs, in male and female mouse retinas. Extracellular spike recordings revealed that DSGCs respond preferentially to either vertical or horizontal bars, those that are perpendicular to their preferred-null motion axes. By contrast, the glutamate input to all four DSGC types measured using whole-cell patch-clamp techniques was found to be tuned along the vertical axis. Tuned glutamatergic excitation was heavily reliant on type 5A bipolar cells, which appear to be electrically coupled via connexin 36 containing gap junctions to the vertically oriented processes of wide-field amacrine cells.Vertically tuned inputs are transformed by the GABAergic/cholinergic =starburst> amacrine cells (SACs), which are critical components of the direction-selective circuit, into distinct patterns of inhibition and excitation. Feed-forward SAC inhibition appears to ‘veto’ preferred orientation glutamate excitation in dorsal/ventral (but not nasal/temporal) coding DSGCs ‘flipping’ their orientation tuning by 90 degrees, and accounts for the apparent mismatch between glutamate input tuning and the DSGC's spiking response. Together, these results reveal how two distinct synaptic motifs interact to generate complex feature selectivity, shedding light on the intricate circuitry that underlies visual processing in the retina.Significance StatementThe classical work of Hubel and Wiesel (1959) demonstrated that neurons in the cat visual cortex are often selective for multiple stimulus features, such as direction and orientation. Here, we show that direction-selective ganglion cells (DSGCs) in the mouse retina are also selective for stimulus orientation, suggesting that multi-feature extraction may begin earlier in the visual system than previously envisioned. Using a combination of patch-clamp, cell-specific genetic KO, and optogenetic strategies, we show that multi-feature coding relies on distinct mechanisms in the nasal/temporal and dorsal/ventral coding DSGC.

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Direction selectivity

Cited by 4 publications

References 104 publications

Starburst amacrine cells form gap junctions in the early postnatal stage of the mouse retina

Starburst amacrine cells form gap junctions in the early postnatal stage of the mouse retina

Spatiotemporal properties of glutamate input support direction selectivity in the dendrites of retinal starburst amacrine cells

Neural Circuits Underlying Multifeature Extraction in the Retina

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