Sensory determinants of behavioral dynamics in Drosophila thermotaxis

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

Volumn 112, Issue 2, 2015, Pages E220-E229

  Klein, Mason ^a   Afonso, Bruno ^a,b   Vonner, Ashley J ^a   Hernandez Nunez, Luis ^a   Berck, Matthew ^a   Tabone, Christopher J ^a   Kane, Elizabeth A ^a   Pieribone, Vincent A ^c,d   Nitabach, Michael N ^c   Cardona, Albert ^b   Zlatic, Marta ^b   Sprecher, Simon G ^b,e   Gershow, Marc ^a   Garrity, Paul A ^f   Samuel, Aravinthan D T ^a,b   Sternberg, Paul W ^g  

^a HARVARD UNIVERSITY   (United States)

^b Janelia Farm Research Campus ^*  (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHN B PIERCE LABORATORY   (United States)

^e UNIVERSITY OF FRIBOURG   (Switzerland)

^f BRANDEIS UNIVERSITY   (United States)

^g CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Calcium imaging; Navigation; Reverse correlation; Temperature; Voltage imaging

Indexed keywords

CALCIUM;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DORSAL ORGAN GANGLION; DROSOPHILA; ELECTRIC POTENTIAL; GANGLION; LARVA; MOLECULAR DYNAMICS; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; SENSATION; SENSITIVITY ANALYSIS; SENSORY ANALYSIS; SENSORY NERVE CELL; STIMULATION; TEMPERATURE; THERMAL ANALYSIS; ANIMAL; CALCIUM SIGNALING; DROSOPHILA MELANOGASTER; LOCOMOTION; PHYSIOLOGY; TEMPERATURE SENSE; THERMORECEPTOR; TRANSGENIC ANIMAL;

ANIMALIA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CALCIUM SIGNALING; DROSOPHILA MELANOGASTER; GANGLIA; LARVA; LOCOMOTION; OPTOGENETICS; THERMORECEPTORS; THERMOSENSING;

EID: 84920936105     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416212112     Document Type: Article

References (45)

1. Lockery SR (2011) The computational worm: Spatial orientation and its neuronal basis in C. elegans. Curr Opin Neurobiol 21(5):782-790.
2. Gomez-Marin A, Duistermars BJ, Frye MA, Louis M (2010) Mechanisms of odor-tracking: Multiple sensors for enhanced perception and behavior. Front Cell Neurosci 4:6.
3. Garrity PA, Goodman MB, Samuel AD, Sengupta P (2010) Running hot and cold: Behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes Dev 24(21):2365-2382.
4. Ramot D, MacInnis BL, Goodman MB (2008) Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat Neurosci 11(8):908-915.
5. Luo L, et al. (2010) Navigational decision making in Drosophila thermotaxis. J Neurosci 30(12):4261-4272.
6. Gershow M, et al. (2012) Controlling airborne cues to study small animal navigation. Nat Methods 9(3):290-296.
7. Gomez-Marin A, Stephens GJ, Louis M (2011) Active sampling and decision making in Drosophila chemotaxis. Nat Commun 2:441.
8. Lahiri S, et al. (2011) Two alternating motor programs drive navigation in Drosophila larva. PLoS ONE 6(8):e23180.
9. Gallio M, Ofstad TA, Macpherson LJ, Wang JW, Zuker CS (2011) The coding of temperature in the Drosophila brain. Cell 144(4):614-624.
10. Hamada FN, et al. (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217-220.
11. RosenzweigM, Kang K, Garrity PA (2008) Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc Natl Acad Sci USA 105(38): 14668-14673.
12. Shen WL, et al. (2011) Function of rhodopsin in temperature discrimination in Drosophila. Science 331(6022):1333-1336.
13. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ (2003) Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 6(3):267-273.
14. Jin L, et al. (2012) Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 75(5):779-785.
15. Ringach D, Shapley R (2004) Reverse correlation in neurophysiology. Cogn Sci 28: 147-166.
16. Kato S, Xu Y, Cho CE, Abbott LF, Bargmann CI (2014) Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics. Neuron 81(3):616-628.
17. Coen P, et al. (2014) Dynamic sensory cues shape song structure in Drosophila. Nature 507(7491):233-237.
18. Rosenzweig M, et al. (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19(4):419-424.
19. Kwon Y, Shen WL, Shim HS, Montell C (2010) Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. J Neurosci 30(31):10465-10471.
20. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505-533.
21. Xiang Y, et al. (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468(7326):921-926.
22. Sprecher SG, Pichaud F, Desplan C (2007) Adult and larval photoreceptors use different mechanisms to specify the same Rhodopsin fates. Genes Dev 21(17):2182-2195.
23. Kane EA, et al. (2013) Sensorimotor structure of Drosophila larva phototaxis. Proc Natl Acad Sci USA 110(40):E3868-E3877.
24. Louis M, Huber T, Benton R, Sakmar TP, Vosshall LB (2008) Bilateral olfactory sensory input enhances chemotaxis behavior. Nat Neurosci 11(2):187-199.
25. Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46(3):445-456.
26. Pfeiffer BD, et al. (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci USA 105(28):9715-9720.
27. Python F, Stocker RF (2002) Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J Comp Neurol 445(4):374-387.
28. Masuda-Nakagawa LM, Gendre N, O'Kane CJ, Stocker RF (2009) Localized olfactory representation in mushroom bodies of Drosophila larvae. Proc Natl Acad Sci USA 106(25): 10314-10319.
29. Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2011) Molecular and cellular organization of the taste system in the Drosophila larva. J Neurosci 31(43):15300-15309.
30. Tian L, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875-881.
31. Klapoetke NC, et al. (2014) Independent optical excitation of distinct neural populations. Nat Methods 11(3):338-346.
32. Clark DA, Freifeld L, Clandinin TR (2013) Mapping and cracking sensorimotor circuits in genetic model organisms. Neuron 78(4):583-595.
33. Bargmann CI, Horvitz HR (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7(5):729-742.
34. Mori I, Ohshima Y (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376(6538):344-348.
35. Bullock TH, Diecke FP (1956) Properties of an infra-red receptor. J Physiol 134(1):47-87.
36. Loftus R, Corbière-Tichané GL (1987) Response of antennal cold receptors of the catopid beetles, Speophyes lucidulus Delar. And Cholera angustata Fab. to very slowly changing temperature. J Comp Physiol 161:399-405.
37. Stocker RF, Singh RN, Schorderet M, Siddiqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232(2):237-248.
38. Hwang RY, et al. (2007) Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr Biol 17(24):2105-2116.
39. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR (2011) Defining the computational structure of the motion detector in Drosophila. Neuron 70(6):1165-1177.
40. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A (2011) Internal structure of the fly elementary motion detector. Neuron 70(6):1155-1164.
41. Cardona A, et al. (2010) An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol 8(10):e1000502.
42. 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.
43. Prevedel R, et al. (2014) Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat Methods 11:727-730.
44. Ahrens MB, et al. (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485(7399):471-477.
45. 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.