Pan-neuronal imaging in roaming Caenorhabditis elegans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 8, 2016, Pages E1082-E1088

  Venkatachalam, Vivek ^a,b   Ji, Ni ^a,b   Wang, Xian ^a,b   Clark, Christopher ^c   Mitchell, James Kameron ^a,b   Klein, Mason ^a,b   Tabone, Christopher J ^a,b   Florman, Jeremy ^c   Ji, Hongfei ^d   Greenwood, Joel ^b   Chisholm, Andrew D ^e   Srinivasan, Jagan ^f   Alkema, Mark ^c   Zhen, Mei ^g,h   Samuel, Aravinthan D T ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d NANJING UNIVERSITY   (China)

^e NEUROBIOLOGY SECTION   (United States)

^f Life Science and Bioengineering Center   (United States)

^g MOUNT SINAI HOSPITAL   (Canada)

^h UNIVERSITY OF TORONTO   (Canada)

Author keywords

C. elegans; Calcium imaging; Drosophila; Thermotaxis

Indexed keywords

RED FLUORESCENT PROTEIN; PHOTOPROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CORRELATIONAL STUDY; DROSOPHILA; ELECTROENCEPHALOGRAM; GANGLION; IMAGING AND DISPLAY; LOCOMOTION; NONHUMAN; PAN NEURONAL IMAGING; PRIORITY JOURNAL; SENSORY STIMULATION; TEMPERATURE; ANIMAL; ANIMAL BEHAVIOR; CELL NUCLEUS; CYTOLOGY; FLUORESCENCE IMAGING; GENETICS; METABOLISM; NERVE CELL; PROCEDURES;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CELL NUCLEUS; GANGLIA, INVERTEBRATE; LOCOMOTION; LUMINESCENT PROTEINS; NEURONS; OPTICAL IMAGING;

EID: 84959254435     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507109113     Document Type: Article

References (46)

1. Faumont S, et al. (2011) An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans. PLoS One 6(9):e24666.
2. Kawano T, et al. (2011) An imbalancing act: Gap junctions reduce the backward motor circuit activity to bias C. elegans for forward locomotion. Neuron 72(4):572-586.
3. Clark DA, Gabel CV, Gabel H, Samuel AD (2007) Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 27(23):6083-6090.
4. Suzuki H, et al. (2003) In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39(6):1005-1017.
5. Chalasani SH, et al. (2007) Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450(7166):63-70.
6. Piggott BJ, Liu J, Feng Z, Wescott SA, Xu XZS (2011) The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell 147(4):922-933.
7. Ahrens MB, et al. (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485(7399):471-477.
8. Flusberg BA, et al. (2008) High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat Methods 5(11):935-938.
9. Katona G, et al. (2012) Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat Methods 9(2):201-208.
10. Holekamp TF, Turaga D, Holy TE (2008) Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57(5):661-672.
11. Grewe BF, Langer D, Kasper H, Kampa BM, Helmchen F (2010) High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat Methods 7(5):399-405.
12. Cheng A, Gonçalves JT, Golshani P, Arisaka K, Portera-Cailliau C (2011) Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing. Nat Methods 8(2):139-142.
13. Deisseroth K, Schnitzer MJ (2013) Engineering approaches to illuminating brain structure and dynamics. Neuron 80(3):568-577.
14. Ziv Y, et al. (2013) Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci 16(3):264-266.
15. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10(5):413-420.
16. Schrödel T, Prevedel R, Aumayr K, Zimmer M, Vaziri A (2013) Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light. Nat Methods 10(10):1013-1020.
17. Prevedel R, et al. (2014) Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat Methods 11(7):727-730.
18. Abrahamsson S, et al. (2013) Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat Methods 10(1):60-63.
19. Kato S, et al. (2015) Global Brain Dynamics Embed the Motor Command Sequence of Caenorhabditis elegans. Cell 163(3):656-669.
20. Chen T-W, et al. (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295-300.
21. Tursun B, Patel T, Kratsios P, Hobert O (2011) Direct conversion of C. elegans germ cells into specific neuron types. Science 331(6015):304-308.
22. Nguyen JP, et al. (2016) Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans. Proc Natl Acad Sci USA 113:E1074-E1081.
23. Klein M, et al. (2015) Sensory determinants of behavioral dynamics in Drosophila thermotaxis. Proc Natl Acad Sci USA 112(2):E220-E229.
24. Faumont S, Lockery SR (2006) The awake behaving worm: Simultaneous imaging of neuronal activity and behavior in intact animals at millimeter scale. J Neurophysiol 95(3):1976-1981.
25. Leifer AM, Fang-Yen C, Gershow M, Alkema MJ, Samuel ADT (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat Methods 8(2): 147-152.
26. Gray J, Lissmann HW, Lissmann HW (1964) The Locomotion of Nematodes. J Exp Biol 41:135-154.
27. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS (2008) Dimensionality and dynamics in the behavior of C. elegans. PLOS Comput Biol 4(4):e1000028.
28. Yemini E, Jucikas T, Grundy LJ, Brown AEX, Schafer WR (2013) A database of Caenorhabditis elegans behavioral phenotypes. Nat Methods 10(9):877-879.
29. Kimura KD, Miyawaki A, Matsumoto K, Mori I (2004) The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14(14):1291-1295.
30. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56(1):110-156.
31. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100(1):64-119.
32. Clark DA, Biron D, Sengupta P, Samuel AD (2006) The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J Neurosci 26(28):7444-7451.
33. Ben Arous J, Tanizawa Y, Rabinowitch I, Chatenay D, Schafer WR (2010) Automated imaging of neuronal activity in freely behaving Caenorhabditis elegans. J Neurosci Methods 187(2):229-234.
34. Wen Q, et al. (2012) Proprioceptive coupling within motor neurons drives C. elegans forward locomotion. Neuron 76(4):750-761.
35. Chronis N, Zimmer M, Bargmann CI (2007) Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4(9):727-731.
36. Guo ZV, Hart AC, Ramanathan S (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods 6(12):891-896.
37. Kim E, Sun L, Gabel CV, Fang-Yen C (2013) Long-term imaging of Caenorhabditis elegans using nanoparticle-mediated immobilization. PLoS One 8(1):e53419.
38. Luo L, et al. (2010) Navigational decision making in Drosophila thermotaxis. J Neurosci 30(12):4261-4272.
39. Gomez-Marin A, Louis M (2012) Active sensation during orientation behavior in the Drosophila larva: More sense than luck. Curr Opin Neurobiol 22(2):208-215.
40. Luo L, et al. (2014) Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proc Natl Acad Sci USA 111(7):2776-2781.
41. Ohnishi N, Kuhara A, Nakamura F, Okochi Y, Mori I (2011) Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO J 30(7): 1376-1388.
42. Beverly M, Anbil S, Sengupta P, Sengupta P (2011) Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans. J Neurosci 31(32):11718-11727.
43. Kuhara A, et al. (2008) Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320(5877):803-807.
44. Biron D, Wasserman S, Thomas JH, Samuel ADT, Sengupta P (2008) An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proc Natl Acad Sci USA 105(31):11002-11007.
45. Hendricks M, Ha H, Maffey N, Zhang Y (2012) Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement. Nature 487(7405):99-103.
46. Altun-Gultekin Z, et al. (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128(11):1951-1969.