Dendro-somatic synaptic inputs to ganglion cells contradict receptive field and connectivity conventions in the mammalian retina

Grimes, William N.; Sedlacek, Miloslav; Musgrove, Morgan; Nath, Amurta; Tian, Hua; Hoon, Mrinalini; Singer, Joshua H.; Diamond, Jeffrey S.

doi:10.1016/j.cub.2021.11.005

Cited by 13 publications

(15 citation statements)

References 86 publications

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“…An example of such a circuitry at the IPL-to-INL border is the perinuclear nests which are formed by dopaminergic amacrine cells around the cell bodies of postsynaptic AII amacrine cells (Voigt and Wassle, 1987; Casini et al, 1995; Contini and Raviola, 2003). Dendro-somatic synaptic interactions were also shown to occur at regular ganglion cell bodies with great functional impact (Grimes et al, 2022) and could represent a circuit motif for amacrine-dRGCs interactions in the INL as well. Furthermore, it is known from a subset of dRGCs to express distinct voltage-gated calcium channel subunits in murine retinas, which were not found in regular RGCs, suggesting that those dRGCs may have distinct functional properties (De Sevilla Müller et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Spatial distribution and functional integration of displaced ipRGCs

Duda,

Block,

Pradhan

et al. 2023

Preprint

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The mammalian retina contains many distinct types of ganglion cells, which form mosaics to evenly tile the retina with cells of each type at each position of the visual field. It is well known that displaced retinal ganglion cells (dRGCs) exist with cell bodies in the inner nuclear layer, along with regularly placed RGCs with cell bodies in the ganglion cell layer. A prominent example of dRGCs are M1-type intrinsically photosensitive ganglion cells (ipRGCs) which exist in various species including humans and non-human primates. Little is known, however, about their spatial relationship with regularly placed ipRGCs. Here, we identified mouse ipRGC types M1, M2, and M4/sONα by immunohistochemistry and light microscopy to anatomically investigate the distribution of displaced and regularly placed cells. Reconstruction of immunolabeled dendritic mosaics from M1 and sONα RGCs indicated that dRGCs tiled the retina evenly with their regularly placed RGC partners. Multi-electrode array recordings revealed conventional receptive fields of displaced sONα RGCs which fit into the functional mosaic of their regularly placed counterparts. We further analyzed the RGC distributions across complete retinas. The analysis of regularly placed M1 ipRGCs and αRGCs revealed distinct density gradients where ~16% and ~8% occurred as dRGCs, respectively. The density distributions of dRGCs showed type-specific patterns which followed neither the global density distribution of all ganglion cells nor the local densities of corresponding cell types. Our study shows that the displacement of ganglion cell bodies into the inner nuclear layer occurs in a type-dependent manner, where dRGCs are positioned to form complete mosaics with their regularly placed RGC partners. Our data suggest that dRGCs and regularly placed RGCs serve the same functional role within their corresponding population of ganglion cells.

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Section: Discussionmentioning

confidence: 99%

Spatial distribution and functional integration of displaced ipRGCs

Duda,

Block,

Pradhan

et al. 2023

Preprint

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“…To probe possible connections between B/K WAC dendrites and bipolar cells, we performed connectomic analyses. We started with an existing dataset, SBEM (scanning block-face electron microscopy) volume k0725 (Ding et al, 2016), in which all of the inhibitory synapses onto an OFF Delta RGC had been annotated and some presynaptic amacrine cells, including WACs, had been traced (Grimes et al, 2022) ( Fig. 6A-C ).…”

Section: Resultsmentioning

confidence: 99%

Molecular identification of wide-field amacrine cells in mouse retina that encode stimulus orientation

Park,

Lei,

Pisano

et al. 2023

Preprint

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SUMMARYVisual information processing is sculpted by a diverse group of inhibitory interneurons in the retina called amacrine cells. Yet, for most of the >60 amacrine cell types, molecular identities and specialized functional attributes remain elusive. Here, we developed an intersectional genetic strategy to target a group of wide-field amacrine cells (WACs) in mouse retina that co-express the transcription factor Bhlhe22 and the Kappa Opioid Receptor (KOR; B/K WACs). B/K WACs feature straight, unbranched dendrites spanning over 0.5 mm (∼15° visual angle) and produce non-spiking responses to either light increments or decrements. Two-photon dendritic population imaging reveals Ca2+signals tuned to the physical orientations of B/K WAC dendrites, signifying a robust structure-function alignment. B/K WACs establish divergent connections with multiple retinal neurons, including unexpected connections with non-orientation-tuned ganglion cells and bipolar cells. Our work sets the stage for future comprehensive investigations of the most enigmatic group of retinal neurons: WACs.

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“…Ca 21 responses were observed in both lobular and arboreal dendrites and were partially blocked by CPP, suggesting that Ca v channels and NMDARs are present in both locations (cf. Grimes et al, 2021). The block evoked by CPP suggests that sufficient glutamate is bound to the NMDARs (cf.…”

Section: Rod Bipolar Input To An Aii Evokes Synaptic Responses In Off...mentioning

confidence: 99%

“…For arboreal dendrites there is evidence for extrasynaptic NMDARs (Veruki et al, 2019) and our results suggest that these processes also express Ca v channels (cf. Grimes et al, 2021). As NMDARs are involved in plasticity of the Cx36-dependent gap junctions between AIIs (Kothmann et al, 2012), depolarization by coincident synaptic inputs could be a mechanism for spatially restricted control of plasticity (cf.…”

Section: Simultaneous Local and Global Integration In Aiismentioning

confidence: 99%

“…Near visual threshold the rod bipolar inputs to an AII may be too weak to evoke measurable output by exocytosis at the lobular dendrites, despite the negative activation threshold of the Ca v channels (À55 mV ;Habermann et al, 2003). Instead, larger-amplitude local EPSPs in the distal arboreal dendrites could evoke output directly onto ganglion cell somata, suggested by recent evidence for chemical synaptic contacts made by arboreal dendrites (Grimes et al, 2021). This could explain that in mouse, rod-driven signals near visual threshold can be measured in some OFF-ganglion cells, but not in OFFcone bipolars (Arman and Sampath, 2012).…”

Section: Electrical Coupling Impacts Global But Not Local Synaptic In...mentioning

confidence: 99%

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Dendritic Morphology of an Inhibitory Retinal Interneuron Enables Simultaneous Local and Global Synaptic Integration

2022

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Amacrine cells, inhibitory interneurons of the retina, feature synaptic inputs and outputs in close proximity throughout their dendritic trees, making them notable exceptions to prototypical somato-dendritic integration with output transmitted via axonal action potentials. The extent of dendritic compartmentalization in amacrine cells with widely differing dendritic tree morphology, however, is largely unexplored. Combining compartmental modeling, dendritic Ca 21 imaging, targeted microiontophoresis and multielectrode patch-clamp recording (voltage and current clamp, capacitance measurement of exocytosis), we investigated integration in the AII amacrine cell, a narrow-field electrically coupled interneuron that participates in multiple, distinct microcircuits. Physiological experiments were performed with in vitro slices prepared from retinas of both male and female rats. We found that the morphology of the AII enables simultaneous local and global integration of inputs targeted to different dendritic regions. Local integration occurs within spatially restricted dendritic subunits and narrow time windows and is largely unaffected by the strength of electrical coupling. In contrast, global integration across the dendritic tree occurs over longer time periods and is markedly influenced by the strength of electrical coupling. These integrative properties enable AII amacrines to combine local control of synaptic plasticity with location-independent global integration. Dynamic inhibitory control of dendritic subunits is likely to be of general importance for amacrine cells, including cells with small dendritic trees, as well as for inhibitory interneurons in other regions of the CNS.

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Dendro-somatic synaptic inputs to ganglion cells contradict receptive field and connectivity conventions in the mammalian retina

Cited by 13 publications

References 86 publications

Spatial distribution and functional integration of displaced ipRGCs

Spatial distribution and functional integration of displaced ipRGCs

Molecular identification of wide-field amacrine cells in mouse retina that encode stimulus orientation

Dendritic Morphology of an Inhibitory Retinal Interneuron Enables Simultaneous Local and Global Synaptic Integration

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