Long-term imaging reveals behavioral plasticity during C. elegans dauer exit
Abstract 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-te...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-022-01471-4 |
| _version_ | 1797980467178242048 |
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| author | Friedrich Preusser Anika Neuschulz Jan Philipp Junker Nikolaus Rajewsky Stephan Preibisch |
| author_facet | Friedrich Preusser Anika Neuschulz Jan Philipp Junker Nikolaus Rajewsky Stephan Preibisch |
| author_sort | Friedrich Preusser |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-11T05:54:52Z |
| format | Article |
| id | doaj.art-efcda652d7cb4e109baea2961ff4d279 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-11T05:54:52Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-efcda652d7cb4e109baea2961ff4d2792022-12-22T04:41:56ZengBMCBMC Biology1741-70072022-12-0120111410.1186/s12915-022-01471-4Long-term imaging reveals behavioral plasticity during C. elegans dauer exitFriedrich Preusser0Anika Neuschulz1Jan Philipp Junker2Nikolaus Rajewsky3Stephan Preibisch4Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)Janelia Research Campus, Howard Hughes Medical InstituteAbstract 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.https://doi.org/10.1186/s12915-022-01471-4Behavioral imagingC. elegans dauerNeuroplasticity |
| spellingShingle | Friedrich Preusser Anika Neuschulz Jan Philipp Junker Nikolaus Rajewsky Stephan Preibisch Long-term imaging reveals behavioral plasticity during C. elegans dauer exit BMC Biology Behavioral imaging C. elegans dauer Neuroplasticity |
| title | Long-term imaging reveals behavioral plasticity during C. elegans dauer exit |
| title_full | Long-term imaging reveals behavioral plasticity during C. elegans dauer exit |
| title_fullStr | Long-term imaging reveals behavioral plasticity during C. elegans dauer exit |
| title_full_unstemmed | Long-term imaging reveals behavioral plasticity during C. elegans dauer exit |
| title_short | Long-term imaging reveals behavioral plasticity during C. elegans dauer exit |
| title_sort | long term imaging reveals behavioral plasticity during c elegans dauer exit |
| topic | Behavioral imaging C. elegans dauer Neuroplasticity |
| url | https://doi.org/10.1186/s12915-022-01471-4 |
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