Focusing on optic tectum circuitry through the lens of genetics

Nevin, Linda M; Robles, Estuardo; Baier, Herwig; Scott, Ethan K.

doi:10.1186/1741-7007-8-126

Cited by 127 publications

(140 citation statements)

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“…The hippocampus is one of the most highly evolved structures in the mammalian brain necessary for many forms of learning and memory and therefore equipped with many compensating mechanisms to maintain its critical functions with the specialized mammalian neocortex. By contrast, the SC continues to subserve most of the functions of localization in space, persistent activity, and initiation of single or multisensory motor output that has been crucial to the survival of the vertebrate line throughout evolution (39,40). However, the SC and its nonmammalian homolog the optic tectum, like most other central nervous system regions, maintain activity-dependent interactions critical to adaptive circuitry during development (41,42).…”

Section: Discussionmentioning

confidence: 99%

Eye opening and PSD95 are required for long-term potentiation in developing superior colliculus

Zhao

Murata

Constantine‐Paton

2012

Proc. Natl. Acad. Sci. U.S.A.

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The only major glutamate receptor membrane-associated guanylate kinase scaffolds expressed in the young superficial superior colliculus (SC) are synapse-associated protein 102 (SAP102) and postsynaptic density protein 95 (PSD95). In this, as in all visual brain regions examined, synaptic PSD95 increases rapidly following simultaneous eyelid opening (EO). We show that EO and PSD95 are necessary for SC NMDA receptor (NMDAR)-dependent long-term potentiation (LTP) and this LTP is eliminated or reinstated by manipulating EO. PSD95 knockdown (KD) in vivo blocks this LTP, but not long-term depression, and reduces frequencies of miniature AMPA receptor and NMDAR currents with no change in presynaptic release. Furthermore, miniature NMDAR currents after PSD95 KD show an activitytriggered calcineurin sensitivity that is normally only found in the pre-EO period when SAP102 binds mixed GluN2A/GluN2B NMDARs. These data indicate that young SC LTP arises from PSD95 unsilencing of silent synapses, that unsilencing is labile in young brain, and that even though SAP102 and PSD95 can bind the same NMDARs, only PSD95 enables SC synaptic maturation.experience-dependent synaptogenesis | pattern vision G enetic knockout (KO) and knockdown (KD) of the dominant postsynaptic density (PSD) glutamate receptor scaffold, membrane-associated guanylate kinase (MAGUK) postsynaptic density protein 95 (PSD95), have been examined intensively for synaptic effects in area CA1 of rodent hippocampus and mostly in older animals or with cultured hippocampal slices. In the hippocampus, the synaptic MAGUKs synapse-associated protein 102 (SAP102), PSD95, and postsynaptic density protein 93 (PSD93) bind ionotropic glutamate receptors and many molecules through which the receptors signal (1-3). A fourth MAGUK, synapseassociated protein 97 (SAP97), binds selectively to AMPA receptor (AMPAR) subunit GluR1 helping to deliver it to, but not remain at the PSD (4).Although the hippocampus is a highly evolved and important brain region, it is unlikely to reflect properties of all other regions that are critical to brain function. Synaptic development has been studied much more intensively in the visual pathway where it differs significantly from the hippocampus because the onset of pattern vision is necessary for completion of its synaptic connectivity (5-7) and it has a critical period in which considerable visual plasticity disappears (8). Moreover, the superficial superior colliculus (SC), central to eye movements and integration of multiple sensory pathways for orientation in space, is the only brainstem region where synaptic MAGUK function has been studied at all, and it is a region where SAP102 and PSD95 are the only significant MAGUK glutamate receptor scaffolds.In rodent visual pathways, SAP102 is the dominant scaffold at the PSD until 2-3 h after controlled eyelid opening (EO) and the onset of pattern vision. At this time, PSD95 in visual synapses increases twofold to threefold (9, 10). This is followed, in the SC where retinal, visual cortical, and thalam...

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Section: Discussionmentioning

confidence: 99%

Eye opening and PSD95 are required for long-term potentiation in developing superior colliculus

Zhao

Murata

Constantine‐Paton

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Organized in a layered structure, the optic tectum (TeO) mediates complex visually evoked behaviors by integrating multisensory information (Nevin et al, 2010 2006). As information is highly processed and filtered within tectal layers, recent research focused more on the investigation of distinct microcircuits (e.g.…”

Section: Optic Tectummentioning

confidence: 99%

Phylogeny and expression divergence of metabotropic glutamate receptor genes in the brain of zebrafish (Danio rerio)

Haug

Gesemann

Mueller

2013

J of Comparative Neurology

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Glutamate, the most abundant excitatory neurotransmitter of the central nervous system, modulates synaptic transmission and neuronal excitability via metabotropic glutamate receptors (mGluRs). These receptors are essential components for diverse cognitive functions and they represent potential drug targets for the treatment of a number of neurological and psychiatric disorders. Here, we describe the phylogenetic relation and mRNA distribution of zebrafish mGluRs. In comparison to the eight mglurs present in the mammalian genome, we identified 13 different mglur genes in the zebrafish genome. In situ hybridization experiments in zebrafish revealed widespread expression patterns for the different mglurs in the central nervous system, implicating their significance in diverse neuronal functions. Prominent mglur expression is found in the olfactory bulb, the optic tectum, the hypothalamus, the cerebellum, and the retina. We show that expression pattern of paralogs generated by the teleost specific whole genome duplication is overlapping in some brain regions but complementary in others, suggesting sub-and/or neofunctionalization in the latter. Group I mglurs are similarly expressed in brain areas of both larval and adult zebrafish, suggesting that their functions are comparable during these stages. AbstractGlutamate, the most abundant excitatory neurotransmitter of the central nervous system, modulates synaptic transmission and neuronal excitability via metabotropic glutamate receptors (mGluRs). These receptors are essential components for diverse cognitive functions and they represent potential drug targets for the treatment of a number of neurological and psychiatric disorders.Here, we describe the phylogenetic relation and mRNA distribution of zebrafish mGluRs. In comparison to the eight mglurs present in the mammalian genome, we identified 13 different mglur genes in the zebrafish genome. In situ hybridization experiments in zebrafish revealed widespread expression patterns for the different mglurs in the central nervous system, implicating their significance in diverse neuronal functions. Prominent mglur expression is found in the olfactory bulb, the optic tectum, the hypothalamus, the cerebellum, and the retina. We show that expression pattern of paralogs generated by the teleost specific whole genome duplication is overlapping in some brain regions but complementary in others, suggesting suband/or neofunctionalization in the latter. Group I mglurs are similarly expressed in brain areas of both larval and adult zebrafish, suggesting that their functions are comparable during these stages.

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“…The tectum in zebrafish is generally believed to be a visual structure, and models of its function have almost exclusively addressed inputs from the retina [112][113][114]. However, the mammalian superior colliculus, which is homologous to the tectum, receives inputs from various brain regions and sensory modalities [115].…”

Section: Summary Of the Problemmentioning

confidence: 99%

Imaging, manipulation and optogenetics in zebrafish

Favre-bulle¹

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This thesis investigates the advantages and limits of using laser light for illumination and micromanipulation of the nervous system deep in-vivo in zebrafish. Further interest in the study neuronal pathways and functions in zebrafish led to employ laser micro-manipulation for the stimulation of the systems of interest and the development of optogenetics system and light sheet microscopy for analyses of the processes. First I present the investigation of the interaction of light and brain tissue as we aim to quantify light scattered in zebrafish brain tissue with depth. This is of great importance for optogenetics as it uses light to control (turn on or off) neurons and the unwanted/scattered light out of the aimed region could significantly affect results of experiments. The measurements and model developed to predict light propagation through brain tissue and how much a focussed beam broadens and alters with depth are presented in details. Results show that illumination of individual neurons is possible at depth in the zebrafish brain, despite scattering that results from shallower neural tissue. This means that the approach presented allows for optogenetics manipulation of single neurons to be performed without optical correction for scattering. Secondly, I construct an optogenetics system where we employ advanced optics and novel algorithm to deliver versatile two dimensional illumination that can be used at any depth in the fish. I present an example of a problem that I have solved, and resulting optogenetics results that were obtained, using this new technology. In chapter 5, I was responsible for the improvements implemented on the optogenetics system and the different tests to show its performances. Lucy Heap has performed multiple experiments on that system and I present one example she performed and the results she got.In chapter 7, I performed the manipulation of free otolith in water. I with Alex Stilgoe performed scanning experiments of otolith on an optical trapping system that Alex Stilgoe built.We both performed the analysis of the experimental results. Alex Stilgoe performed the force modelisation with Ray optics methods and we compared it with experimental results. Statement of parts of the thesis submitted to qualify for the award of another degreeNone. I have special thanks to Shu, Swaantje and Lucy for our philosophical discussions, the sharing of our experiences in the good and bad moments of our PhDs and their support.Finally I have some friends that I would like to thank for their great support without necessarily realising it: Mari-wenn, Estelle and Arnaud.8 ABSTRACT

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Focusing on optic tectum circuitry through the lens of genetics

Cited by 127 publications

References 98 publications

Eye opening and PSD95 are required for long-term potentiation in developing superior colliculus

Eye opening and PSD95 are required for long-term potentiation in developing superior colliculus

Phylogeny and expression divergence of metabotropic glutamate receptor genes in the brain of zebrafish (Danio rerio)

Imaging, manipulation and optogenetics in zebrafish

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