Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients

Clark, Damon A.; Gabel, Christopher V.; Gabel, Harrison W.; Samuel, Aravinthan D. T.

doi:10.1523/jneurosci.1032-07.2007

Cited by 101 publications

(88 citation statements)

References 22 publications

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“…Several classes of GECIs have performed well for neural imaging, encompassing single-FP and FRET sensors, and sensors based on calmodulin and troponin-C calcium-binding domains. Published GECIs are adequate for detecting high frequency bursts of neuronal activity, making them appropriate for activity localization in mouse myotubes (Nakai et al, 2001), mouse cerebellum (Diez-Garcia et al, 2005), or in invertebrate systems (Kerr et al, 2000;Higashijima et al, 2003;Wang et al, 2003;Chronis et al, 2007;Clark et al, 2007). However, reliable in vivo single-AP detection is not yet feasible with the current generation of techniques.…”

Section: Resultsmentioning

confidence: 99%

Reporting neural activity with genetically encoded calcium indicators

2008

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Genetically encoded calcium indicators (GECIs), based on recombinant fluorescent proteins, have been engineered to observe calcium transients in living cells and organisms. Through observation of calcium, these indicators also report neural activity. We review progress in GECI construction and application, particularly toward in vivo monitoring of sparse action potentials (APs). We summarize the extrinsic and intrinsic factors that influence GECI performance. A simple model of GECI response to AP firing demonstrates the relative significance of these factors. We recommend a standardized protocol for evaluating GECIs in a physiologically relevant context. A potential method of simultaneous optical control and recording of neuronal circuits is presented.

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Section: Resultsmentioning

confidence: 99%

Reporting neural activity with genetically encoded calcium indicators

2008

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“…Our goal was to determine whether our setup was capable of finding distinct neuronal activity patterns that correspond to sensory input and motor output. To activate the circuits for thermotaxis in C. elegans, which are most sensitive at temperatures near and above the temperature of cultivation, we cultivated worms at 15°C and subjected them to fluctuations between 15°C and 17.5°C (3,29). To extract general patterns in calcium dynamics across the head ganglia, we performed cluster analysis.…”

Section: Classification and Correlation Of Intracellular Calcium Dynamentioning

confidence: 99%

“…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.

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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“…Calcium imaging of the AFD neuron in response to temperature waveforms has shown that the operating range of AFD spans the range of isothermal tracking and cryophilic behavior. At temperatures near and above the T s , warming will depolarize AFD and cause an increase in intracellular calcium level whereas cooling will hyperpolarize AFD and cause a decrease in the calcium levels (29)(30)(31)(32).…”

Section: Afd Responds To Temperatures That Span Both Negative and Posmentioning

confidence: 99%

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Luo

Cook

Venkatachalam

et al. 2014

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

100

116

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The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (T s ) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above T s (negative thermotaxis) and performs isothermal tracking near T s . Under some conditions, the worm migrates up temperature gradients below T s (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward T s to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below T s . We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.N avigational behaviors provide a framework for exploring the interplay among sensorimotor circuits, learning, and memory. During a navigational task, animals eventually reach their goals by implementing strategies composed of sensorimotor rules. Experience can modify navigational goals, so memory can also be integrated into sensorimotor pathways. Studying navigation in the nematode Caenorhabditis elegans offers the possibility of understanding the plasticity and programming of sensorimotor circuits from input to output in a small nervous system (1).Previous studies established C. elegans thermotaxis as a model for experience-dependent navigation (2-6). When worms are exposed to specific temperatures between 15°C and 25°C for at least 4 h, they adopt those temperatures as their thermotactic setpoint (T s ) (2, 3, 5, 7). When placed on a spatial temperature gradient, worms seek the T s . When arriving near T s , worms track isotherms. Genetic analysis of thermotaxis has yielded mutants that are athermotactic (crawling randomly on temperature gradients), cryophilic (crawling to the coldest point on a temperature gradient irrespective of T s ), or thermophilic (crawling to the warmest point on a temperature gradient). This observation led to the suggestion that thermotaxis might involve separate circuits for negative thermotaxis (movement down gradients) and positive thermotaxis (movement up gradients) that balance near T s (2, 4).Systematic laser ablation a...

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Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients

Cited by 101 publications

References 22 publications

Reporting neural activity with genetically encoded calcium indicators

Reporting neural activity with genetically encoded calcium indicators

Pan-neuronal imaging in roaming Caenorhabditis elegans

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

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