A genetically encoded reporter of synaptic activity in vivo

Dreosti, Elena; Odermatt, Benjamin; Dorostkar, Mario M.; Lagnado, Leon

doi:10.1038/nmeth.1399

Cited by 203 publications

(223 citation statements)

References 33 publications

(50 reference statements)

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“…However, until now it has not been widely used probably because it is not easy to analyze the calcium transient with a poor signal-to-noise ratio. GCaMP1.6 and GCaMP2 were successfully used to detect calcium signals in the neuropil of the zebrafish tectum, which consisted of axonal arbors of retinal ganglion cells and dendritic arbors of the tectal cells (26,27). In contrast to these studies, our present study clearly demonstrated that GCaMP-HS can detect calcium signals in both the cell bodies and neurites.…”

Section: Alternating and Synchronized Periodic Activation Of The Motorcontrasting

confidence: 66%

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Muto

Ohkura

Kotani

et al. 2011

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

177

150

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Animal behaviors are generated by well-coordinated activation of neural circuits. In zebrafish, embryos start to show spontaneous muscle contractions at 17 to 19 h postfertilization. To visualize how motor circuits in the spinal cord are activated during this behavior, we developed GCaMP-HS (GCaMP-hyper sensitive), an improved version of the genetically encoded calcium indicator GCaMP, and created transgenic zebrafish carrying the GCaMP-HS gene downstream of the Gal4-recognition sequence, UAS (upstream activation sequence). Then we performed a gene-trap screen and identified the SAIGFF213A transgenic fish that expressed Gal4FF, a modified version of Gal4, in a subset of spinal neurons including the caudal primary (CaP) motor neurons. We conducted calcium imaging using the SAIGFF213A; UAS:GCaMP-HS double transgenic embryos during the spontaneous contractions. We demonstrated periodic and synchronized activation of a set of ipsilateral motor neurons located on the right and left trunk in accordance with actual muscle movements. The synchronized activation of contralateral motor neurons occurred alternately with a regular interval. Furthermore, a detailed analysis revealed rostral-to-caudal propagation of activation of the ipsilateral motor neuron, which is similar to but much slower than the rostrocaudal delay observed during swimming in later stages. Our study thus demonstrated coordinated activities of the motor neurons during the first behavior in a vertebrate. We propose the GCaMP technology combined with the Gal4FF-UAS system is a powerful tool to study functional neural circuits in zebrafish.neuronal activity | calcium transient | transgenesis | Tol2 | gene trapping V ertebrate behaviors are generated by coordinated activation of neural networks. The zebrafish provides an excellent system to study the neural activities of vertebrates because of its transparency and external development. It has been reported that zebrafish embryos show a first locomotive activity as early as 17 h postfertilization (hpf), which is called spontaneous contraction or coiling; namely, they spontaneously contract the left and right trunk muscles alternatively without any external stimulus. This behavior precedes touch-evoked escape response and swimming, which emerge in later developmental stages (1). The neuronal activities during the spontaneous contractions were analyzed by electrophysiological approaches, and periodic and synchronized depolarization of the spinal neurons has been observed (2, 3). However, it is still challenging to analyze the activity of a neural network by electrophysiology because it requires recording from multiple neurons by using multiple electrodes. To understand how functional neural circuits are formed and operated, a new technology to monitor the activity of multiple neurons is desired.An alternative approach to record activities from multiple neurons is to detect Ca 2+ influx associated with generation of action potentials. For this purpose, fluorescent calcium-indicator dyes, which should be introdu...

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Section: Alternating and Synchronized Periodic Activation Of The Motorcontrasting

confidence: 66%

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Muto

Ohkura

Kotani

et al. 2011

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

177

150

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“…Here, by imaging presynaptic Ca 2+ 17 and mitochondrial positioning in multiple terminals of the same axon, we show that mitochondrial occupancy determines presynaptic Ca 2+ responses and can also affect vesicular release. Moreover, we demonstrate that mitochondrial localisation at presynaptic terminals is tuned by long‐term changes in network activity dependent on Miro1‐mediated mitochondrial trafficking.…”

Section: Introductionmentioning

confidence: 85%

Miro1‐dependent mitochondrial positioning drives the rescaling of presynaptic Ca ²⁺ signals during homeostatic plasticity

et al. 2016

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Mitochondrial trafficking is influenced by neuronal activity, but it remains unclear how mitochondrial positioning influences neuronal transmission and plasticity. Here, we use live cell imaging with the genetically encoded presynaptically targeted Ca2+ indicator, SyGCaMP5, to address whether presynaptic Ca2+ responses are altered by mitochondria in synaptic terminals. We find that presynaptic Ca2+ signals, as well as neurotransmitter release, are significantly decreased in terminals containing mitochondria. Moreover, the localisation of mitochondria at presynaptic sites can be altered during long‐term activity changes, dependent on the Ca2+‐sensing function of the mitochondrial trafficking protein, Miro1. In addition, we find that Miro1‐mediated activity‐dependent synaptic repositioning of mitochondria allows neurons to homeostatically alter the strength of presynaptic Ca2+ signals in response to prolonged changes in neuronal activity. Our results support a model in which mitochondria are recruited to presynaptic terminals during periods of raised neuronal activity and are involved in rescaling synaptic signals during homeostatic plasticity.

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“…Because of the prominent role of calmodulin in a variety of Ca 2þ -dependent pathways, including long-term potentiation (39), extending previously obtained results to cooperative buffering is important. Better tools for describing cooperative buffering may also help in interpreting imaging data obtained with the latest genetically encoded calmodulin-derived Ca 2þ indicator dyes (40)(41)(42)(43). More accurate description of binding dynamics of these dyes may help in increasing the temporal resolution of Ca 2þ imaging obtained using these synthetic buffers.…”

Section: Discussionmentioning

confidence: 99%

Padé Approximation of a Stationary Single-Channel Ca 2+ Nanodomain

Matveev

2016

Biophysical Journal

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We consider the stationary solution for the Ca 2þ concentration near a point Ca 2þ source describing a single-channel Ca 2þ nanodomain, in the presence of a single mobile buffer with one-to-one Ca 2þ binding stoichiometry. Previously, a number of Ca 2þ nanodomains approximations have been developed, for instance the excess buffer approximation (EBA), the rapid buffering approximation (RBA), and the linear approximation (LIN), each valid for appropriate buffering conditions. Apart from providing a simple method of estimating Ca 2þ and buffer concentrations without resorting to computationally expensive numerical solution of reaction-diffusion equations, such approximations proved useful in revealing the dependence of nanodomain Ca 2þ distribution on crucial parameters such as buffer mobility and its Ca 2þ binding properties. In this study, we present a different form of analytic approximation, which is based on matching the shortrange Taylor series of the nanodomain concentration with the long-range asymptotic series expressed in inverse powers of distance from channel location. Namely, we use a ''dual'' Padé rational function approximation to simultaneously match terms in the short-and the long-range series, and we show that this provides an accurate approximation to the nanodomain Ca 2þ and buffer concentrations. We compare this approximation with the previously obtained approximations and show that it yields a better estimate of the free buffer concentration for a wide range of buffering conditions. The drawback of our method is that it has a complex algebraic form for any order higher than the lowest bilinear order, and cannot be readily extended to multiple Ca 2þ channels. However, it may be possible to extend the Padé method to estimate Ca 2þ nanodomains in the presence of cooperative Ca 2þ buffers with two Ca 2þ binding sites, the case that existing methods do not address.

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A genetically encoded reporter of synaptic activity in vivo

Cited by 203 publications

References 33 publications

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Miro1‐dependent mitochondrial positioning drives the rescaling of presynaptic Ca ²⁺ signals during homeostatic plasticity

Padé Approximation of a Stationary Single-Channel Ca 2+ Nanodomain

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A genetically encoded reporter of synaptic activity in vivo

Cited by 203 publications

References 33 publications

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish

Miro1‐dependent mitochondrial positioning drives the rescaling of presynaptic Ca 2+ signals during homeostatic plasticity

Padé Approximation of a Stationary Single-Channel Ca 2+ Nanodomain

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Miro1‐dependent mitochondrial positioning drives the rescaling of presynaptic Ca ²⁺ signals during homeostatic plasticity