Targeted Optical Probing of Neuronal Circuit Dynamics Using Fluorescent Protein Sensors

Qiu, De-Lai; Akemann, Walther; Chu, Chun-Ping; Araki, Rikita; Knöpfel, Thomas

doi:10.1159/000123039

Cited by 14 publications

(11 citation statements)

References 58 publications

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“…It will be of interest to see whether neighboring release sites to different postsynaptic cells may be individually regulated, both in terms of presynaptic modulation of transmitter release and in terms of synaptic plasticity. To this end, development of new calcium probes (Qiu et al, 2008), perhaps targetable to active zones, would be of importance, and to further analyse the spatial activation of branched, complex presynaptic terminals, voltage sensitive indicators (Qui et al, 2008) might be useful.…”

Section: Discussionmentioning

confidence: 99%

Presynaptic calcium signalling in cerebellar mossy fibres

Thomsen

Jörntell

Midtgaard

2010

Front. Neural Circuits

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Whole-cell recordings were obtained from mossy fibre terminals in adult turtles in order to characterize the basic membrane properties. Calcium imaging of presynaptic calcium signals was carried out in order to analyse calcium dynamics and presynaptic GABA B inhibition. A tetrodotoxin (TTX)-sensitive fast Na + spike faithfully followed repetitive depolarizing pulses with little change in spike duration or amplitude, while a strong outward rectification dominated responses to long-lasting depolarizations. High-threshold calcium spikes were uncovered following addition of potassium channel blockers. Calcium imaging using Calcium-Green dextran revealed a stimulus-evoked all-or-none TTX-sensitive calcium signal in simple and complex rosettes. All compartments of a complex rosette were activated during electrical activation of the mossy fibre, while individual simple and complex rosettes along an axon appeared to be isolated from one another in terms of calcium signalling. CGP55845 application showed that GABA B receptors mediated presynaptic inhibition of the calcium signal over the entire firing frequency range of mossy fibres. A paired-pulse depression of the calcium signal lasting more than 1 s affected burst firing in mossy fibres; this paired-pulse depression was reduced by GABA B antagonists. While our results indicated that a presynaptic rosette electrophysiologically functioned as a unit, topical GABA application showed that calcium signals in the branches of complex rosettes could be modulated locally, suggesting that cerebellar glomeruli may be dynamically sub-compartmentalized due to ongoing inhibition mediated by Golgi cells. This could provide a fine-grained control of mossy fibre-granule cell information transfer and synaptic plasticity within a mossy fibre rosette.

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Section: Discussionmentioning

confidence: 99%

Presynaptic calcium signalling in cerebellar mossy fibres

Thomsen

Jörntell

Midtgaard

2010

Front. Neural Circuits

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“…These indicators have the advantage of being fast reporters which can be targeted to specific cellular compartments like the ER and the mitochondria [107; 108]. Studies investigating changes in calcium homeostasis using large arrays of cells are also now providing new in vivo results, but only in a limited number of studies in AD models [27; 29; 109].…”

Section: Cellular Calcium Transients Have a Dendritic Originmentioning

confidence: 99%

Calcium's role as nuanced modulator of cellular physiology in the brain

Frazier

Maimaiti

Anderson

et al. 2017

Biochemical and Biophysical Research Communications

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Neuroscientists studying normal brain aging, spinal cord injury, Alzheimer’s disease (AD) and other neurodegenerative diseases have focused considerable effort on carefully characterizing intracellular perturbations in calcium dynamics or levels. At the cellular level, calcium is known for controlling life and death and orchestrating most events in between. For many years, intracellular calcium has been recognized as an essential ion associated with nearly all cellular functions from cell growth to degeneration. Often the emphasis is on the negative impact of calcium dysregulation and the typical worse-case-scenario leading inevitably to cell death. However, even high amplitude calcium transients, when executed acutely can alter neuronal communication and synaptic strength in positive ways, without necessarily killing neurons. Here, we focus on the evidence that calcium has a subtle and distinctive role in shaping and controlling synaptic events that underpin neuronal communication and that these subtle changes in aging or AD may contribute to cognitive decline. We emphasize that calcium imaging in dendritic components is ultimately necessary to directly test for the presence of age- or disease-associated alterations during periods of synaptic activation.

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“…21 indicators is widely used to record transient Ca 21 increases associated with bioelectrical activity in single neurons or multiple neurons simultaneously (Cossart et al, 2005;Qiu et al, 2008). The photoproteins aequorin and obelin are bioluminescent complexes, which emit light upon Ca 21 binding (Shimomura et al, 1962;Morin and Hastings, 1971a;Wilson and Hastings, 1998).…”

Section: Imaging Of Camentioning

confidence: 99%

“…Most of the recent Ca 21 imaging studies rely on fluorescence microscopy of synthetic or genetically encoded indicators (Cossart et al, 2005;Qiu et al, 2008). The latter indicators, which can be targeted to specific neuronal populations, consist of a fusion protein incorporating GFP or its spectral variants and a Ca 21 -binding protein (Mank and Griesbeck, 2008).…”

Section: Imaging Of Camentioning

confidence: 99%

Calcium imaging in single neurons from brain slices using bioluminescent reporters

Drobac

Tricoire

Chaffotte

et al. 2009

J of Neuroscience Research

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Responses of three bioluminescent Ca(2+) sensors were studied in vitro and in neurons from brain slices. These sensors consisted of tandem fusions of green fluorescent protein (GFP) with the photoproteins aequorin, obelin, or a mutant aequorin with high Ca(2+) sensitivity. Kinetics of GFP-obelin responses to a saturating Ca(2+) concentration were faster than those of GFP-aequorin at all Mg(2+) concentrations tested, whereas GFP-mutant aequorin responses were the slowest. GFP-photoproteins were efficiently expressed in pyramidal neurons following overnight incubation of acute neocortical slices with recombinant Sindbis viruses. Expression of GFP-photoproteins did not result in conspicuous modification of morphological or electrophysiological properties of layer V pyramidal cells. The three sensors allowed the detection of Ca(2+) transients associated with action potential discharge in single layer V pyramidal neurons. In these neurons, depolarizing steps of increasing amplitude elicited action potential discharge of increasing frequency. Bioluminescent responses of the three sensors were similar in several respects: detection thresholds, an exponential increase with stimulus intensity, photoprotein consumptions, and kinetic properties. These responses, which were markedly slower than kinetics measured in vitro, increased linearly during the action potential discharge and decayed exponentially at the end of the discharge. Onset slopes increased with stimulus intensity, whereas decay kinetics remained constant. Dendritic light emission contributed to whole-field responses, but the spatial resolution of bioluminescence imaging was limited to the soma and proximal apical dendrite. Nonetheless, the high signal-to-background ratio of GFP-photoproteins allowed the detection of Ca(2+) transients associated with 5 action potentials in single neurons upon whole-field bioluminescence recordings.

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Targeted Optical Probing of Neuronal Circuit Dynamics Using Fluorescent Protein Sensors

Cited by 14 publications

References 58 publications

Presynaptic calcium signalling in cerebellar mossy fibres

Presynaptic calcium signalling in cerebellar mossy fibres

Calcium's role as nuanced modulator of cellular physiology in the brain

Calcium imaging in single neurons from brain slices using bioluminescent reporters

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