The Neural Circuits and Synaptic Mechanisms Underlying Motor Initiation in C. elegans

Piggott, Beverly J.; Liu, Jie; Feng, Zhaoyang; Wescott, Seth A.; Xu, X.Z. Shawn

doi:10.1016/j.cell.2011.08.053

Cited by 269 publications

(393 citation statements)

References 47 publications

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“…The AVA interneurons are important to initiate backward movements (23)(24)(25)(26). We found that expression of the dbl-1 coding region using the nmr-1 promoter, whose expression overlaps with dbl-1 expression only in AVA, significantly rescued the learning defect in dbl-1(nk3) mutant animals ( Fig.…”

Section: Dbl-1 Produced By the Ava Command Interneurons Promotes Avermentioning

confidence: 67%

“…S5 A and B). Because calcium influx of AVA is correlated with the initiation of spontaneous backward movements (26,35,36), we recorded AVA calcium dynamics of animals in the nematode growth medium (NGM) buffer using a microfluidic device that allows generation of body waves, which result in forward or backward movements (36). We measured the G-CaMP fluorescence intensity in AVA in naive and PA14-trained animals and calculated the rate of intensity change (Fig.…”

Section: Dbl-1 Signals To the Hypodermis To Direct Aversive Olfactorymentioning

confidence: 99%

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DBL-1, a TGF-β, is essential for Caenorhabditis elegans aversive olfactory learning

Zhang¹,

Zhang

2012

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

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The TGF-β superfamily is conserved throughout metazoan, and its members play essential roles in development and disease. TGF-β has also been implicated in adult neural plasticity. However, the underlying mechanisms are not well understood. Here we report that DBL-1, a Caenorhabditis elegans TGF-β homolog known to control body morphology and immunity, is essential for aversive olfactory learning of potentially harmful bacteria food. We show that DBL-1 generated by the AVA command interneurons, which are critical for sensorimotor responses, regulates aversive olfactory learning, and that the activity of the type I TGF-β receptor SMA-6 in the hypodermis is needed during adulthood to generate olfactory plasticity. These spatial and temporal mechanisms are critical for the DBL-1 signaling to achieve its diverse functions in development and adult neural plasticity. Interestingly, aversive training decreases AVA calcium response, leading to an increase in the DBL-1 signal secreted from AVA, revealing an experience-dependent change that can underlie the role of TGF-β signaling in mediating plasticity.experience-dependent secretion | molecular and cellular mechanisms for TGF-beta pathway in learning

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Section: Dbl-1 Produced By the Ava Command Interneurons Promotes Avermentioning

confidence: 67%

Section: Dbl-1 Signals To the Hypodermis To Direct Aversive Olfactorymentioning

confidence: 99%

DBL-1, a TGF-β, is essential for Caenorhabditis elegans aversive olfactory learning

Zhang¹,

Zhang

2012

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

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“…The nematode Caenorhabditis elegans is particularly ideal for optical neurophysiology owing to its small size, optical transparency, compact nervous system, and ease of genetic manipulation. Imaging systems for tracking the activity of small numbers of neurons have been effective in determining their role during nematode locomotion and navigational behaviors like chemotaxis, thermotaxis, and the escape response (1)(2)(3)(4)(5)(6).…”

mentioning

confidence: 99%

Pan-neuronal imaging in roaming Caenorhabditis elegans

Venkatachalam

et al. 2015

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

221

216

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We present an imaging system for pan-neuronal recording in crawling Caenorhabditis elegans. A spinning disk confocal microscope, modified for automated tracking of the C. elegans head ganglia, simultaneously records the activity and position of ∼80 neurons that coexpress cytoplasmic calcium indicator GCaMP6s and nuclear localized red fluorescent protein at 10 volumes per second. We developed a behavioral analysis algorithm that maps the movements of the head ganglia to the animal's posture and locomotion. Image registration and analysis software automatically assigns an index to each nucleus and calculates the corresponding calcium signal. Neurons with highly stereotyped positions can be associated with unique indexes and subsequently identified using an atlas of the worm nervous system. To test our system, we analyzed the brainwide activity patterns of moving worms subjected to thermosensory inputs. We demonstrate that our setup is able to uncover representations of sensory input and motor output of individual neurons from brainwide dynamics. Our imaging setup and analysis pipeline should facilitate mapping circuits for sensory to motor transformation in transparent behaving animals such as C. elegans and Drosophila larva.C. elegans | Drosophila | calcium imaging | thermotaxis U nderstanding how brain dynamics creates behaviors requires quantifying the flow and transformation of sensory information to motor output in behaving animals. Optical imaging using genetically encoded calcium or voltage fluorescent probes offers a minimally invasive method to record neural activity in intact animals. The nematode Caenorhabditis elegans is particularly ideal for optical neurophysiology owing to its small size, optical transparency, compact nervous system, and ease of genetic manipulation. Imaging systems for tracking the activity of small numbers of neurons have been effective in determining their role during nematode locomotion and navigational behaviors like chemotaxis, thermotaxis, and the escape response (1-6).Recordings from large numbers of interconnected neurons are required to understand how neuronal ensembles carry out the systematic transformations of sensory input into motor patterns that build behavioral decisions.Several methods for fast 3D imaging of neural activity in a fixed imaging volume have been developed for different model organisms (7)(8)(9)(10)(11)(12)(13)(14). High-speed light sheet microscopy, light field microscopy, multifocus microscopy, and two-photon structured illumination microscopy have proved effective for rapidly recording large numbers of neurons in immobilized, intact, transparent animals like larval zebrafish and nematodes (15)(16)(17)(18)(19). However, these methods are problematic when attempting to track many neurons within the bending and moving body of a behaving animal. Panneuronal recording in moving animals poses higher demands on spatial and temporal resolution. Furthermore, extracting neuronal signals from recordings in a behaving animal requires an effective analysis pipel...

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“…In C. elegans, nociceptive sensations and avoidance have been intensively studied. However, the reported studies were focused on the functional mapping of the connections among sensory neurons and interneurons, using cell ablation, optogenetic manipulation and in vivo calcium imaging [4][5][6][7] . Therefore, the peripheral modulation of nociceptive sensations and avoidance behaviours is poorly understood.…”

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confidence: 99%

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

et al. 2015

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Sensory modulation is essential for animal sensations, behaviours and survival. Peripheral modulations of nociceptive sensations and aversive behaviours are poorly understood. Here we identify a biased cross-inhibitory neural circuit between ASH and ASI sensory neurons. This inhibition is essential to drive normal adaptive avoidance of a CuSO 4 (Cu 2 þ ) challenge in Caenorhabditis elegans. In the circuit, ASHs respond to Cu 2 þ robustly and suppress ASIs via electro-synaptically exciting octopaminergic RIC interneurons, which release octopamine (OA), and neuroendocrinally inhibit ASI by acting on the SER-3 receptor. In addition, ASIs sense Cu 2 þ and permit a rapid onset of Cu 2 þ -evoked responses in Cu 2 þ -sensitive ADF neurons via neuropeptides possibly, to inhibit ASHs. ADFs function as interneurons to mediate ASI inhibition of ASHs by releasing serotonin (5-HT) that binds with the SER-5 receptor on ASHs. This elaborate modulation among sensory neurons via reciprocal inhibition fine-tunes the nociception and avoidance behaviour.

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The Neural Circuits and Synaptic Mechanisms Underlying Motor Initiation in C. elegans

Cited by 269 publications

References 47 publications

DBL-1, a TGF-β, is essential for Caenorhabditis elegans aversive olfactory learning

DBL-1, a TGF-β, is essential for Caenorhabditis elegans aversive olfactory learning

Pan-neuronal imaging in roaming Caenorhabditis elegans

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

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