A high-throughput method to deliver targeted optogenetic stimulation to moving C. elegans populations

Liu, Mochi; Kumar, Sandeep; Sharma, Anuj Kumar; Leifer, Andrew M.

doi:10.1371/journal.pbio.3001524

Cited by 16 publications

(44 citation statements)

References 75 publications

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“…The modular nature of our system allows for the integration of more advanced opto-electronics or software components (e.g. optogenetics (49) or other tracking software (50, 51)). Moreover, given its cost (<150$) and straightforward assembly, the platform can be considered for larger screens involving several microscopes running in parallel.…”

Section: Discussionmentioning

confidence: 99%

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

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Neuschulz

Junker

et al. 2022

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During their lifetime, animals must adapt their behavior to survive in changing environments. This ability requires the nervous system to adjust through dynamic expression of neurotransmitters and receptors but also through growth, spatial reorganization and connectivity while integrating external stimuli. For instance, despite having a fixed neuronal cell lineage, the nematode Caenorhabditis elegans’ nervous system remains plastic throughout its development. Here, we focus on a specific example of nervous system plasticity, the C. elegans dauer exit decision. Under unfavorable conditions, larvae will enter the non-feeding and non-reproductive dauer stage and adapt their behavior to cope with a new environment. Upon improved conditions, this stress resistant developmental stage is actively reversed to resume reproductive development. However, how different environmental stimuli regulate the exit decision mechanism and thereby drive the larva’s behavioral change is unknown. To fill this gap, we developed a new open hardware method for long-term imaging (12h) of C. elegans larvae. We identified dauer-specific behavioral motifs and characterized the behavioral trajectory of dauer exit in different environments to identify key decision points. Combining long-term behavioral imaging with transcriptomics, we find that bacterial ingestion triggers a change in neuropeptide gene expression to establish post-dauer behavior. Taken together, we show how a developing nervous system can robustly integrate environmental changes, activate a developmental switch and adapt the organism’s behavior to a new environment.

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Section: Discussionmentioning

confidence: 99%

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Preußer

Neuschulz

Junker

et al. 2022

Preprint

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show abstract

“…A description of the workflow, including detailed instructions, can be accessed under [ 22 ]. The modular nature of our system allows for the integration of more advanced opto-electronics or software components (e.g., optogenetics [ 51 ] or other tracking software [ 52 , 53 ]). Moreover, given its cost (< 150$) and straightforward assembly, the platform can be considered for larger screens involving several microscopes running in parallel.…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

et al. 2022

View full text Add to dashboard Cite

Background During their lifetime, animals must adapt their behavior to survive in changing environments. This ability requires the nervous system to undergo adjustments at distinct temporal scales, from short-term dynamic changes in expression of neurotransmitters and receptors to longer-term growth, spatial and connectivity reorganization, while integrating external stimuli. The nematode Caenorhabditis elegans provides a model of nervous system plasticity, in particular its dauer exit decision. Under unfavorable conditions, larvae will enter the non-feeding and non-reproductive stress-resistant dauer stage and adapt their behavior to cope with the harsh new environment, with active reversal under improved conditions leading to resumption of reproductive development. However, how different environmental stimuli regulate the exit decision mechanism and thereby drive the larva’s behavioral change is unknown. To fill this gap and provide insights on behavioral changes over extended periods of time, we developed a new open hardware method for long-term imaging (12h) of C. elegans larvae. Results Our WormObserver platform comprises open hardware and software components for video acquisition, automated processing of large image data (> 80k images/experiment) and data analysis. We identified dauer-specific behavioral motifs and characterized the behavioral trajectory of dauer exit in different environments and genetic backgrounds to identify key decision points and stimuli promoting dauer exit. Combining long-term behavioral imaging with transcriptomics data, we find that bacterial ingestion triggers a change in neuropeptide gene expression to establish post-dauer behavior. Conclusions Taken together, we show how a developing nervous system can robustly integrate environmental changes activate a developmental switch and adapt the organism’s behavior to a new environment. WormObserver is generally applicable to other research questions within and beyond the C. elegans field, having a modular and customizable character and allowing assessment of behavioral plasticity over longer periods.

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“…We discovered that animals traveling forward are much more likely to respond to a mechanosensory stimulus by backing up (reversal), than animals that receive the same stimulus while they are in the middle of a turn. In other words the worm's response to mechanosensory stimuli is gated by the animal's short-timescale behavioral context [16,17]. Suppressing mechanosensory-evoked reversals during turns may be part of a prey avoidance strategy.…”

Section: Introductionmentioning

confidence: 99%

“…We used a high-throughput closed-loop optogenetic approach [17] to interrogate the mechanosensorimotor circuitry in C. elegans and measured the animal's behavior in response to over 39,000 stimulus events. From these measurements, we identified a putative circuit by which inhibitory signals from turning-associated neurons disrupt mechanosensory processing and modulates the likelihood of a reversal depending on the animal's behavior.…”

Section: Introductionmentioning

confidence: 99%

Inhibitory motor signals gate mechanosensory processing in C. eleagns

Kumar¹,

Sharma²,

Leifer³

2023

Preprint

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Animals must integrate sensory cues with their current behavioral context to generate a suitable response, but how this integration occurs is poorly understood. Here we report that Caenorhabditis elegans uses inhibitory signals from turning-associated neurons to rapidly modulate mechanosensory processing depending on the animal's behavioral context. Using high-throughput optogenetic perturbations triggered on behavior, we show that turning associated neurons SAA, RIV and/or SMB suppress mechanosensory-evoked reversals during turns. We find that activation of the gentle-touch mechanosensory neurons or of any of the interneurons AIZ, RIM, AIB and AVE during a turn is less likely to evoke a reversal than activation during forward movement. Adding inhibition of SAA, RIV and SMB during a turn restores the likelihood with which mechanosensory activation evokes reversals. Seperately, activation of premotor interneuron AVA evokes reversals regardless of whether the animal is turning or moving forward. We therefore propose that inhibitory signals from SAA, RIV and/or SMB gate mechanosensory signals upstream of neuron AVA, and identify putative synapses and receptors where this gating occurs. We conclude that C. elegans relies on inhibitory feedback from the motor circuit to modulate its response to sensory stimuli on fast timescales. This need for motor signals in sensory processing may explain the ubiquity of motor-related neural activity patterns across the brain, including in sensory processing areas.

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A high-throughput method to deliver targeted optogenetic stimulation to moving C. elegans populations

Cited by 16 publications

References 75 publications

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Long-term imaging reveals behavioral plasticity during C. elegans dauer exit

Inhibitory motor signals gate mechanosensory processing in C. eleagns

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