Neural engineering with photons as synaptic transmitters

Porta-de-la-Riva, Montserrat; Gonzalez, Adriana Carolina; Sanfeliu-Cerdán, Neus; Karimi, Shadi; Malaiwong, Nawaphat; Pidde, Aleksandra; Morales-Curiel, Luis-Felipe; Fernández, Pablo; González-Bolívar, Sara; Hurth, Cédric; Krieg, Michael

doi:10.1038/s41592-023-01836-9

Cited by 6 publications

(9 citation statements)

References 87 publications

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“…4 ). Two different systems have been established, consisting of the functional interaction of a postsynaptic channelrhodopsin with photons emitted either from calcium-dependent presynaptic luciferases 95 or from secreted constitutively active luciferases. 96 Transsynaptic activation of a photosensitive channelrhodopsin was established in the nematode C. elegans , taking advantage of the known wiring connections and previous functional characterization of the nocifensive nose touch circuit.…”

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

“…4(a) ]. 95 The calcium sensitivity of the luciferase ensured that light emission occurred primarily when the pre-synaptic calcium concentration was high, e.g., during neuronal activity. This synchronized the photon emission precisely to endogenous events, while preventing the rapid depletion of the substrate that may take place with unregulated, constitutively active luciferases 1 and/or the inactivation of the enzymatic activity due to rapid catalysis.…”

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

“… 40 To demonstrate the versatility of PhAST, the concept was applied to different circuits in C. elegans aiming to suppress the endogenous pain response using a green-tuned inhibitory anion channelrhodopsins (ACR1) coupled to a green-emitting eNL and to rewire a circuit mediating the attractive behavior into an avoidance response. 95 …”

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

“…Because Interluminescence requires vesicle release at primarily synaptic sites, de novo generation of asynaptic connections needs to be further demonstrated. In PhAST, the luciferases are distributed throughout the neuron and may not necessarily be confined to the presynapse (unless specifically concentrated there using synaptogyrin tags 95 ), and thus, the transient photon emission might activate neighboring neurons expressing channelrhodopsin in a fashion similar to neurotransmission.…”

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

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Bioluminescence as a functional tool for visualizing and controlling neuronal activity in vivo

Porta-de-la-Riva,

Morales-Curiel,

Carolina Gonzalez

et al. 2024

Neurophoton.

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. The use of bioluminescence as a reporter for physiology in neuroscience is as old as the discovery of the calcium-dependent photon emission of aequorin. Over the years, luciferases have been largely replaced by fluorescent reporters, but recently, the field has seen a renaissance of bioluminescent probes, catalyzed by unique developments in imaging technology, bioengineering, and biochemistry to produce luciferases with previously unseen colors and intensity. This is not surprising as the advantages of bioluminescence make luciferases very attractive for noninvasive, longitudinal in vivo observations without the need of an excitation light source. Here, we review how the development of dedicated and specific sensor-luciferases afforded, among others, transcranial imaging of calcium and neurotransmitters, or cellular metabolites and physical quantities such as forces and membrane voltage. Further, the increased versatility and light output of luciferases have paved the way for a new field of functional bioluminescence optogenetics, in which the photon emission of the luciferase is coupled to the gating of a photosensor, e.g., a channelrhodopsin and we review how they have been successfully used to engineer synthetic neuronal connections. Finally, we provide a primer to consider important factors in setting up functional bioluminescence experiments, with a particular focus on the genetic model Caenorhabditis elegans , and discuss the leading challenges that the field needs to overcome to regain a competitive advantage over fluorescence modalities. Together, our paper caters to experienced users of bioluminescence as well as novices who would like to experience the advantages of luciferases in their own hand.

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Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

Section: Functional Control Over Neuronal Activity With Bioluminescencementioning

confidence: 99%

See 2 more Smart Citations

Bioluminescence as a functional tool for visualizing and controlling neuronal activity in vivo

Porta-de-la-Riva,

Morales-Curiel,

Carolina Gonzalez

et al. 2024

Neurophoton.

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“…The first devices accomplished tasks such as noninvasive animal immobilization without the use of tissue adhesives ( Hulme et al , 2007 ) and long-term culture for longitudinal studies during development ( Keil et al , 2017 ) and ageing ( Xian et al , 2013 ). More complex designs integrate animal immobilization with the presentation of defined stimuli and simultaneous microscopy to investigate the neuronal response to chemicals ( Chronis et al , 2007 ), electrical fields ( Rezai et al , 2010 ), gasses ( Gray et al , 2005 ; Hu et al , 2015 ), thermal ( Gonzales et al , 2019 ), and mechanical stimuli ( Cho et al , 2017 ; Nekimken et al , 2017 ; Setty et al , 2022 ; Porta-de-la Riva et al , 2023 ; and Sanfeliu-cerdán et al , 2023 ). Several devices have been developed and deployed to investigate how C. elegans senses olfactory stimuli.…”

Section: Introductionmentioning

confidence: 99%

Automated dual olfactory device for studying head/tail chemosensation in Caenorhabditis elegans

Karimi,

Gat,

Agazzi

et al. 2024

APL Bioengineering

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The correct interpretation of threat and reward is important for animal survival. Often, the decisions underlying these behavioral programs are mediated by volatile compounds in the animal's environment, which they detect and discriminate with specialized olfactory neurons along their body. Caenorhabditis (C.) elegans senses chemical stimuli with neurons located in the head and the tail of the animal, which mediate either attractive or aversive behaviors. How conflicting stimuli are processed in animals navigating different chemical gradients is poorly understood. Here, we conceived, created, and capitalized on a novel microfluidic device to enable automated and precise stimulation of head and tail neurons, either simultaneously or sequentially, while reading out neuronal activity in sensory and interneurons using genetically encoded calcium indicators. We achieve robust and programmable chemical pulses through the modulation of inlet pressures. To evaluate the device performance, we synchronized the flow control with microscopy data acquisition and characterized the flow properties in the fabricated devices. Together, our design has the potential to provide insight into the neural circuits and behavior of C. elegans simulating the experience of natural environments.

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A MEC-2/stomatin condensate liquid-to-solid phase transition controls neuronal mechanotransduction during touch sensing

Sanfeliu-Cerdán,

Català-Castro,

Mateos

et al. 2023

Nat Cell Biol

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A growing body of work suggests that the material properties of biomolecular condensates ensuing from liquid–liquid phase separation change with time. How this aging process is controlled and whether the condensates with distinct material properties can have different biological functions is currently unknown. Using Caenorhabditis elegans as a model, we show that MEC-2/stomatin undergoes a rigidity phase transition from fluid-like to solid-like condensates that facilitate transport and mechanotransduction, respectively. This switch is triggered by the interaction between the SH3 domain of UNC-89 (titin/obscurin) and MEC-2. We suggest that this rigidity phase transition has a physiological role in frequency-dependent force transmission in mechanosensitive neurons during body wall touch. Our data demonstrate a function for the liquid and solid phases of MEC-2/stomatin condensates in facilitating transport or mechanotransduction, and a previously unidentified role for titin homologues in neurons.

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Neural engineering with photons as synaptic transmitters

Cited by 6 publications

References 87 publications

Bioluminescence as a functional tool for visualizing and controlling neuronal activity in vivo

Bioluminescence as a functional tool for visualizing and controlling neuronal activity in vivo

Automated dual olfactory device for studying head/tail chemosensation in Caenorhabditis elegans

A MEC-2/stomatin condensate liquid-to-solid phase transition controls neuronal mechanotransduction during touch sensing

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