Optical Stimulation of Zebrafish Hair Cells Expressing Channelrhodopsin-2

Monesson-Olson, Bryan D.; Browning-Kamins, Jenna; Aziz-Bose, Razina; Kreines, Fabiana M.; Trapani, Josef G.

doi:10.1371/journal.pone.0096641

Cited by 15 publications

(10 citation statements)

References 49 publications

(71 reference statements)

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“…Optically induced escapes were kinematically similar to those induced by taps, but the angle of the initial C-bend was lower (Figures S3D and S3E), in agreement with reports that electrical stimulation of the M-cell alone gives rise to less effective escapes [25]. The latency from onset of blue light to behavior was long and variable (70 ± 30 ms, mean ± standard deviation, Figure 4F), which is not unusual for ChR2-mediated behavior [26–28] (but see [29]). The effectiveness of blue light correlated with escape latencies across fish (Figures S3F, S3G and S3H) and likely reflects ChR2 expression levels.…”

Section: Resultssupporting

confidence: 90%

A Convergent and Essential Interneuron Pathway for Mauthner-Cell-Mediated Escapes

et al. 2015

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The Mauthner cell (M-cell) is a command-like neuron in teleost fish whose firing in response to aversive stimuli is correlated with short-latency escapes [1-3]. M-cells have been proposed as evolutionary ancestors of startle response neurons of the mammalian reticular formation [4], and studies of this circuit have uncovered important principles in neurobiology that generalize to more complex vertebrate models [3]. The main excitatory input was thought to originate from multisensory afferents synapsing directly onto the M-cell dendrites [3]. Here, we describe an additional, convergent pathway that is essential for the M-cell-mediated startle behavior in larval zebrafish. It is composed of excitatory interneurons called spiral fiber neurons, which project to the M-cell axon hillock. By in vivo calcium imaging, we found that spiral fiber neurons are active in response to aversive stimuli capable of eliciting escapes. Like M-cell ablations, bilateral ablations of spiral fiber neurons largely eliminate short-latency escapes. Unilateral spiral fiber neuron ablations shift the directionality of escapes and indicate that spiral fiber neurons excite the M-cell in a lateralized manner. Their optogenetic activation increases the probability of short-latency escapes, supporting the notion that spiral fiber neurons help activate M-cell-mediated startle behavior. These results reveal that spiral fiber neurons are essential for the function of the M-cell in response to sensory cues and suggest that convergent excitatory inputs that differ in their input location and timing ensure reliable activation of the M-cell, a feedforward excitatory motif that may extend to other neural circuits

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Section: Resultssupporting

confidence: 90%

A Convergent and Essential Interneuron Pathway for Mauthner-Cell-Mediated Escapes

et al. 2015

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“…In order to maintain precise control of stimulus onset, duration and intensity, we examined optically evoked C‐starts using transgenic larvae ( Tg(myo6b:ChR2‐EYFP) ) with stable expression of the light‐gated ion channel Channelrhodopsin‐2 (ChR2) in hair cells of both the auditory and lateral line systems (Monesson‐Olson et al . a ). By using optical stimulation, we could deliver similar stimulation protocols and intensities across our whole‐animal and single afferent neuron experiments.…”

Section: Resultsmentioning

confidence: 99%

Intensity‐dependent timing and precision of startle response latency in larval zebrafish

Troconis

Ordoobadi

Sommers

et al. 2016

The Journal of Physiology

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Key pointsr Using high-speed videos time-locked with whole-animal electrical recordings, simultaneous measurement of behavioural kinematics and field potential parameters of C-start startle responses allowed for discrimination between short-latency and long-latency C-starts (SLCs vs. LLCs) in larval zebrafish.r Apart from their latencies, SLC kinematics and SLC field potential parameters were intensity independent.r Increasing stimulus intensity increased the probability of evoking an SLC and decreased mean SLC latencies while increasing their precision; subtraction of field potential latencies from SLC latencies revealed a fixed time delay between the two measurements that was intensity independent.r The latency and the precision in the latency of the SLC field potentials were linearly correlated to the latencies and precision of the first evoked action potentials (spikes) in hair-cell afferent neurons of the lateral line.r Together, these findings indicate that first spike latency (FSL) is a fast encoding mechanism that can serve to precisely initiate startle responses when speed is critical for survival. AbstractVertebrates rely on fast sensory encoding for rapid and precise initiation of startle responses. In afferent sensory neurons, trains of action potentials (spikes) encode stimulus intensity within the onset time of the first evoked spike (first spike latency; FSL) and the number of evoked spikes. For speed of initiation of startle responses, FSL would be the more advantageous mechanism to encode the intensity of a threat. However, the intensity dependence of FSL and spike number and whether either determines the precision of startle response initiation is not known. Here, we examined short-latency startle responses (SLCs) in larval zebrafish and tested the hypothesis that first spike latencies and their precision (jitter) determine the onset time and precision of SLCs. We evoked startle responses via activation of Channelrhodopsin (ChR2) expressed in ear and lateral line hair cells and acquired high-speed videos of head-fixed larvae while simultaneously recording underlying field potentials. This method allowed for discrimination between primary SLCs and less frequent, long-latency startle responses (LLCs). Quantification of SLC kinematics and field potential parameters revealed that, apart from their latencies, they were intensity independent. We found that increasing stimulus intensity decreased SLC latencies while increasing their precision, which was significantly correlated with corresponding changes in field potential latencies and their precision. Single afferent neuron recordings from the lateral line revealed a similar intensity-dependent decrease in first spike latencies and their jitter, which could account for the intensity-dependent changes in timing and precision of startle response latencies. Abbreviations ChR2, Channelrhodopsin-2; FP, field potential; FP max amplitude, maximum peak-to-peak amplitude of the first biphasic peak observed; FSL, first spike latency; LLC, long-latency C-start...

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“…Optogenetics have been utilised to further our unders-tanding of neural disorders [ 36 ], understand neural systems and encoding [ 37 ] and there is interest in using optogenetics to treat blindness and Parkinson’s disease [ 17 , 38 , 39 ]. Despite the power of these tools and their importance in the field of neuroscience, the potential for use in bionic devices or treatment of conditions in humans is currently limited.…”

Section: Optogenetics and Photoactive Moleculesmentioning

confidence: 99%

Optical Stimulation of Neurons

Thompson

Stoddart

Jansen

2015

CMI

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Our capacity to interface with the nervous system remains overwhelmingly reliant on electrical stimulation devices, such as electrode arrays and cuff electrodes that can stimulate both central and peripheral nervous systems. However, electrical stimulation has to deal with multiple challenges, including selectivity, spatial resolution, mechanical stability, implant-induced injury and the subsequent inflammatory response. Optical stimulation techniques may avoid some of these challenges by providing more selective stimulation, higher spatial resolution and reduced invasiveness of the device, while also avoiding the electrical artefacts that complicate recordings of electrically stimulated neuronal activity. This review explores the current status of optical stimulation techniques, including optogenetic methods, photoactive molecule approaches and infrared neural stimulation, together with emerging techniques such as hybrid optical-electrical stimulation, nanoparticle enhanced stimulation and optoelectric methods. Infrared neural stimulation is particularly emphasised, due to the potential for direct activation of neural tissue by infrared light, as opposed to techniques that rely on the introduction of exogenous light responsive materials. However, infrared neural stimulation remains imperfectly understood, and techniques for accurately delivering light are still under development. While the various techniques reviewed here confirm the overall feasibility of optical stimulation, a number of challenges remain to be overcome before they can deliver their full potential.

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Optical Stimulation of Zebrafish Hair Cells Expressing Channelrhodopsin-2

Cited by 15 publications

References 49 publications

A Convergent and Essential Interneuron Pathway for Mauthner-Cell-Mediated Escapes

A Convergent and Essential Interneuron Pathway for Mauthner-Cell-Mediated Escapes

Intensity‐dependent timing and precision of startle response latency in larval zebrafish

Optical Stimulation of Neurons

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