Cell-Specific Cre Recombinase Expression Allows Selective Ablation of Glutamate Receptors from Mouse Horizontal Cells

Ströh, Sebastian; Sonntag, Stephan; Janssen‐Bienhold, Ulrike; Schultz, Konrad; Cimiotti, Kerstin; Weiler, Reto; Willecke, Klaus; Dedek, Karin

doi:10.1371/journal.pone.0083076

Cited by 22 publications

(24 citation statements)

References 56 publications

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“…However, the functional presence of both AMPA and kainate receptors has been shown in human retinal horizontal cells (Shen et al ., ). More recently, electrophysiological studies in transgenic mice with horizontal cell‐specific ablation of GluA4 (GluA4 fl/fl:Cx57+/Cre) have revealed a small contribution of kainate receptors to glutamate‐induced currents (Ströh et al ., ).…”

Section: Discussionmentioning

confidence: 97%

Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina

Feigenspan¹,

Babai

2015

Eur J of Neuroscience

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As all visual information is represented in the spatio-temporal dynamics of transmitter release from photoreceptors and the combined postsynaptic responses of second-order neurons, appropriate synaptic transfer functions are fundamental for a meaningful perception of the visual world. The functional contribution of horizontal cells to gain control and organization of bipolar and ganglion cell receptive fields can only be evaluated with an in-depth understanding of signal processing in horizontal cells. Therefore, a horizontal slice preparation of the mouse retina was established to record from horizontal cell bodies with their dendritic fields intact and receiving functional synaptic input from cone photoreceptors. Horizontal cell bodies showed spontaneous excitatory currents (spEPSCs) of monophasic and more complex multi-peak waveforms. spEPSCs were induced by quantal release of glutamate from presynaptic cones with a unitary amplitude of 3 pA. Non-stationary noise analysis revealed that spEPSCs with a monoexponential decay were mediated by 7-8 glutamate receptors with a single-channel amplitude of 1.55 pA. Responses to photopic full-field illumination were characterized by reduction of a tonic inward current or hyperpolarization, inhibition of spEPSCs, followed by a fast and transient inward current at light offset. The response to periodic dark/light transitions of different frequencies was dependent on the adaptational status of the cell with a limiting frequency of 10 Hz. Both on and off components of the light response were mediated by AMPA and kainate receptors. Detailed analysis of horizontal cell synaptic physiology is a prerequisite for understanding signal coding and processing at the photoreceptor ribbon synapse.

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Section: Discussionmentioning

confidence: 97%

Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina

Feigenspan¹,

Babai

2015

Eur J of Neuroscience

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Section: Discussionmentioning

confidence: 99%

“…Most previous studies show AMPA‐type glutamate receptors to be the predominant form of glutamate receptor in mammalian HCs, with dense clusters localized below cone and rod terminals and only a small fraction localized to the invaginating tips of dendritic or axon terminal processes (Haverkamp et al, ; Pan and Massey, ). Targeted knockout of AMPA receptor GluA4 in mouse HCs reveals a very small, persistent glutamate receptor current, amounting to just a few percent of the glutamate‐induced current in isolated cells, attributable to kainate receptors (Stroh et al, ). Thus the kainate receptor GluR6/7 likely serves a very limited but potentially specialized role in HC signaling.…”

Section: Discussionmentioning

confidence: 99%

“…It is important to consider that receptor desensitization may significantly influence the behavior of kainate receptors on HCs. In isolated HCs from gluA4 knockout mice, kainate receptor currents were almost completely desensitized until potentiated by the addition of the lectin concanavalin A (Stroh et al, ). In general, kainate receptors are desensitized rapidly upon exposure to glutamate, and kainate receptors deep in the invaginated synaptic cleft of photoreceptors might be expected to be substantially desensitized in the continued presence of glutamate at the dark, resting state in the retina.…”

Section: Discussionmentioning

confidence: 99%

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Membrane‐associated guanylate kinase scaffolds organize a horizontal cell synaptic complex restricted to invaginating contacts with photoreceptors

Vila

Whitaker

O’Brien

2016

J of Comparative Neurology

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Synaptic processes and plasticity of synapses are mediated by large suites of proteins. In most cases, many of these proteins are tethered together by synaptic scaffold proteins. Scaffold proteins have a large number and typically a variety of protein interaction domains that allow many different proteins to be assembled into functional complexes. As each scaffold protein has a different set of protein interaction domains and a unique set of interacting partners, the presence of synaptic scaffolds can provide insight into the molecular mechanisms that regulate synaptic processes. In studies of rabbit retina, we found SAP102 and Chapsyn110 selectively localized in the tips of B-type horizontal cell processes where they contact cone and rod photoreceptors. We further identified some known SAP102 binding partners, kainate receptor GluR6/7 and inward rectifier potassium channel Kir2.1, closely associated with SAP102 in photoreceptor invaginations. The kainate receptor occupies a position distinct from that of the majority of AMPA receptors that dominate the horizontal cell post-synaptic response. GluR6/7 and Kir2.1 presumably are involved in synaptic processes that govern cell-to-cell communication, and could both contribute in different ways to synaptic currents that mediate feedback signaling. Notably, we failed to find evidence for the presence of Cx57 or Cx59 that might be involved in ephaptic feedback signaling in this complex. The presence of SAP102 and its binding partners in both cone and rod invaginating synapses suggests that whatever mechanism is supported by this protein complex is present in both types of photoreceptors.

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“…; Ströh et al . ; Feigenspan & Babai, ). In turn, HCs feed back onto cones and modulate their glutamate release.…”

Section: Introductionmentioning

confidence: 99%

How do horizontal cells ‘talk’ to cone photoreceptors? Different levels of complexity at the cone–horizontal cell synapse

Chapot

Euler

Schubert

2017

The Journal of Physiology

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The first synapse of the retina plays a fundamental role in the visual system. Due to its importance, it is critical that it encodes information from the outside world with the greatest accuracy and precision possible. Cone photoreceptor axon terminals contain many individual synaptic sites, each represented by a presynaptic structure called a 'ribbon'. These synapses are both highly sophisticated and conserved. Each ribbon relays the light signal to one ON cone bipolar cell and several OFF cone bipolar cells, while two dendritic processes from a GABAergic interneuron, the horizontal cell, modulate the cone output via parallel feedback mechanisms. The presence of these three partners within a single synapse has raised numerous questions, and its anatomical and functional complexity is still only partially understood. However, the understanding of this synapse has recently evolved, as a consequence of progress in understanding dendritic signal processing and its role in facilitating global versus local signalling. Indeed, for the downstream retinal network, dendritic processing in horizontal cells may be essential, as they must support important functional operations such as contrast enhancement, which requires spatial averaging of the photoreceptor array, while at the same time preserving accurate spatial information. Here, we review recent progress made towards a better understanding of the cone synapse, with an emphasis on horizontal cell function, and discuss why such complexity might be necessary for early visual processing.

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Cell-Specific Cre Recombinase Expression Allows Selective Ablation of Glutamate Receptors from Mouse Horizontal Cells

Cited by 22 publications

References 56 publications

Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina

Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina

Membrane‐associated guanylate kinase scaffolds organize a horizontal cell synaptic complex restricted to invaginating contacts with photoreceptors

How do horizontal cells ‘talk’ to cone photoreceptors? Different levels of complexity at the cone–horizontal cell synapse

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