Temperature Sensing by an Olfactory Neuron in a Circuit Controlling Behavior of
            <i>C. elegans</i>

Kuhara, Atsushi; Okumura, Minoru; Kimata, Tsubasa; Tanizawa, Yoshinori; Takano, Ryo; Kimura, Koutarou D.; Inada, Hitoshi; Matsumoto, Kunihiro; Mori, Ikue

doi:10.1126/science.1148922

Cited by 190 publications

(247 citation statements)

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“…The AFD neuron has been shown to be the dominant thermosensory neuron in C. elegans, required for all modes of thermotaxis (40,41). Although spontaneous activity in other sensory neurons have been shown to be modulated by temperature changes, only AFD phase locks its calcium dynamics to a rapidly oscillating temperature waveform in a behaving animal (32,(42)(43)(44). Our recordings confirm that the thermosensory response is largely localized to AFDL and AFDR.…”

Section: Discussionsupporting

confidence: 66%

Pan-neuronal imaging in roaming Caenorhabditis elegans

Venkatachalam

et al. 2015

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

215

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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Section: Discussionsupporting

confidence: 66%

Pan-neuronal imaging in roaming Caenorhabditis elegans

Venkatachalam

et al. 2015

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

215

216

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“…Olfactory neuron AWC has recently been included as a secondary thermosensory neuron (Biron et al 2008;Kuhara et al 2008). Depending on the specifics of the experimental procedure, AWC was shown to respond either deterministically to thermal stimuli above a threshold temperature corresponding to the cultivation temperature (Kuhara et al 2008) or stochastically with calcium events whose frequency was stimulus correlated in a manner dependent upon cultivation temperature (Biron et al 2008). The response properties of AFD and AWC provide a cellular correlate for the memory of previous cultivation temperature.…”

Section: Smell As the Conditioned Stimulusmentioning

confidence: 99%

“…Downstream from thermosensation, the DGK-3 diacylglycerol kinase appears to be acting in AFD as a thermal memory molecule modulating the temperature range of synaptic output , and the neuron-specific calcium sensor, NCS-1, functions in AIY to mediate isothermal tracking (Gomez et al 2001). Olfactory neuron AWC has recently been included as a secondary thermosensory neuron (Biron et al 2008;Kuhara et al 2008). Depending on the specifics of the experimental procedure, AWC was shown to respond either deterministically to thermal stimuli above a threshold temperature corresponding to the cultivation temperature (Kuhara et al 2008) or stochastically with calcium events whose frequency was stimulus correlated in a manner dependent upon cultivation temperature (Biron et al 2008).…”

Section: Smell As the Conditioned Stimulusmentioning

confidence: 99%

“…The sensory neurons themselves store a memory of the previous cultivation temperature (Kimura et al 2004;Kuhara et al 2008). AFD responds to thermal stimuli above a threshold temperature, which is dependent upon the cultivation temperature, e.g., 158C, 178C, and 218C for animals cultivated at 158C, 208C, and 258C, respectively ).…”

Section: Smell As the Conditioned Stimulusmentioning

confidence: 99%

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An elegant mind: Learning and memory in Caenorhabditis elegans

Ardiel¹,

Rankin²

2010

Learn. Mem.

275

191

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This article reviews the literature on learning and memory in the soil-dwelling nematode Caenorhabditis elegans. Paradigms include nonassociative learning, associative learning, and imprinting, as worms have been shown to habituate to mechanical and chemical stimuli, as well as learn the smells, tastes, temperatures, and oxygen levels that predict aversive chemicals or the presence or absence of food. In each case, the neural circuit underlying the behavior has been at least partially described, and forward and reverse genetics are being used to elucidate the underlying cellular and molecular mechanisms. Several genes have been identified with no known role other than mediating behavior plasticity.Historically, it was believed that even if they were capable of learning, the nervous systems of invertebrates were too different to be instructive on human cognition. In the 1960s, Kandel and colleagues began studying learning in the marine mollusc Aplysia (Kandel and Tauc 1965). Using this system, they were able to relate behavioral plasticity to changes at specific synapses of identified neurons, and began a biochemical analysis of these neuronal changes, uncovering a role for cAMP, PKA, and CREB. In the 1970s, Benzer and colleagues began a genetic dissection of learning in the fruit fly Drosophila melanogaster (Quinn et al. 1974;Dudai et al. 1976). They established an associative learning assay (Quinn et al. 1974) and conducted a forward genetic screen, identifying the first learning mutant, dunce (Dudai et al. 1976). Since then, many genes have been cloned, and the biological basis of learning has proven to be highly conserved (Barco et al. 2006;Skoulakis and Grammenoudi 2006). Today there is no question as to the relevance of invertebrate research in the field of learning and memory.At about the same time that Kandel was beginning his work with Aplysia, Sydney Brenner chose Caenorhabditis elegans as the organism in which to study development and the nervous system (Brenner 1974). Today this transparent nematode is the world's best understood animal. It's small size ( 1 mm), short life cycle (,3 d), and ease of cultivation make it perfect for the laboratory, and its mode of reproduction is ideal for genetic analysis-selffertilizing hermaphrodites can be easily inbred or crossed with males. The genome has been mapped and sequenced, and there are thousands of mutants and RNAi constructs readily available for researchers. Furthermore, C. elegans has an invariant cell lineage and relatively simple morphology-959 cells make up the entire adult hermaphrodite (Sulston and Horvitz 1977;Sulston et al. 1983). Using serial section electron micrographs, White et al. (1986) were able to construct a neural wiring diagram of the hermaphrodite's 302 neurons. They found about 5000 chemical synapses, 600 gap junctions, and 2000 neuromuscular junctions, the location of which were fairly consistent between animals. With its invariant cell lineage and reproducible connectome, C. elegans was initially viewed as a genetically hardwired ...

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“…Primers designed to the upstream of the predicted start codon of pde-1 (4,765 bp upstream of T04D3.3a), pde-2 (4,721 bp upstream of R08D7.6a), pde-3 (3,030 bp upstream of These behaviors involve at least three pairs of bipolar thermoreceptor neurons: AFD, AWC, and ASI neurons (Mori and Ohshima, 1995;Biron et al, 2008;Kuhara et al, 2008;Beverly et al, 2011). This study concerns the AFD neurons, whose sensory dendrites terminate in a specialized ending comprised of a primary cilium and an extensive array of microvilli (Ward et al, 1975;White et al, 1986).…”

Section: Thermal Migration Assaymentioning

confidence: 99%