Seeing the whole picture: A comprehensive imaging approach to functional mapping of circuits in behaving zebrafish

Neuroscience

Volumn 296, Issue , 2015, Pages 26-38

  Feierstein, C E ^a   Portugues, R ^b   Orger, M B ^a  

^a CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Behavior; Neural circuits; Sensorimotor circuits; Whole brain imaging; Zebrafish

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; BRAIN; BRAIN MAPPING; GENETICS; NERVE CELL; NEUROSCIENCE; PHYSIOLOGY; PROCEDURES; ZEBRA FISH;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BRAIN MAPPING; MODELS, ANIMAL; NEURONS; NEUROSCIENCES; ZEBRAFISH;

EID: 84939972889     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.11.046     Document Type: Review

References (160)

1. Abe G., Suster M.L., Kawakami K. Tol2-mediated transgenesis, gene trapping, enhancer trapping, and the Gal4-UAS system 2011, Elsevier Inc. 3rd ed.
2. Adrian E.D. The impulses produced by sensory nerve endings: Part I. J Physiol 1926, 61:49-72.
3. Agetsuma M., Aizawa H., Aoki T., Nakayama R., Takahoko M., Goto M., Sassa T., Amo R., Shiraki T., Kawakami K., Hosoya T., Higashijima S.-I., Okamoto H. The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 2010, 13:1354-1356.
4. Ahrens M.B., Li J.M., Orger M.B., Robson D.N., Schier A.F., Engert F., Portugues R. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 2012, 485:471-477.
5. Ahrens M.B., Orger M.B., Robson D.N., Li J.M., Keller P.J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Meth 2013, 10:413-420.
6. Aizenberg M., Schuman E.M. Cerebellar-dependent learning in larval zebrafish. J Neurosci 2011, 31:8708-8712.
7. Akerboom J., et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 2012, 32:13819-13840.
8. Ampatzis K., Song J., Ausborn J., Manira El A. Pattern of innervation and recruitment of different classes of motoneurons in adult zebrafish. J Neurosci 2013, 33:10875-10886.
9. Andermann M.L., Kerlin A.M., Reid R.C. Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing. Front Cell Neurosci 2010.
10. Aoki T., Kinoshita M., Aoki R., Agetsuma M., Aizawa H., Yamazaki M., Takahoko M., Amo R., Arata A., Higashijima S.-I., Tsuboi T., Okamoto H. Imaging of neural ensemble for the retrieval of a learned behavioral program. Neuron 2013, 1-14.
11. Asakawa K., Suster M.L., Mizusawa K., Nagayoshi S., Kotani T., Urasaki A., Kishimoto Y., Hibi M., Kawakami K. Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 2008, 105:1255-1260.
12. Baden T., Esposti F., Nikolaev A., Lagnado L. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr Biol 2011, 21:1859-1869.
13. 2+ dynamics underlying sound processing in an auditory interneurone. J Neurobiol 2007, 67:68-80.
14. Bagnall M.W., McLean D.L. Modular organization of axial microcircuits in zebrafish. Science 2014, 343:197-200.
15. Bargmann C.I., Horvitz H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 1991, 7:729-742.
16. Bargmann C.I., Marder E. From the connectome to brain function. Nat Meth 2013, 10:483-490.
17. Beck J.C., Gilland E., Tank D.W., Baker R. Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 2004, 92:3546-3561.
18. Ben Arous J., Tanizawa Y., Rabinowitch I., Chatenay D., Schafer W.R. Automated imaging of neuronal activity in freely behaving Caenorhabditis elegans. J Neurosci Methods 2010, 187:229-234.
19. Bianco I.H., Carl M., Russell C., Clarke J.D.W., Wilson S.W. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev 2008, 3:9.
20. Bollmann J.H., Engert F. Subcellular topography of visually driven dendritic activity in the vertebrate visual system. Neuron 2009, 61:895-905.
21. Borst A., Egelhaaf M. In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc Natl Acad Sci USA 1992, 89:4139-4143.
22. Bozza T., McGann J.P., Mombaerts P., Wachowiak M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 2004, 42:9-21.
23. Briggman K.L., Abarbanel H.D.I., Kristan W.B. Optical imaging of neuronal populations during decision-making. Science 2005, 307:896-901.
24. Briscoe J., Pierani A., Jessell T.M., Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 2000, 101:435-445.
25. Brown E.N., Kass R.E., Mitra P.P. Multiple neural spike train data analysis: state-of-the-art and future challenges. Nat Publ Group 2004, 7:456-461.
26. Broxton M., Grosenick L., Yang S., Cohen N., Andalman A., Deisseroth K., Levoy M. Wave optics theory and 3-D deconvolution for the light field microscope. Opt Express 2013, 21:25418.
27. Burrill J.D., Easter S.S. Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J Comp Neurol 1994, 346:583-600.
28. Büttner-Ennever J.A., Horn A.K. Anatomical substrates of oculomotor control. Curr Opin Neurobiol 1997, 7:872-879.
29. Caron S.J.C., Ruta V., Abbott L.F., Axel R. Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 2013, 497:113-117.
30. Chalfie M., Sulston J.E., White J.G., Southgate E., Thomson J.N., Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 1985, 5:956-964.
31. Chen T.-W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., Looger L.L., Svoboda K., Kim D.S. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
32. Churchland M.M., Yu B.M., Sahani M., Shenoy K.V. Techniques for extracting single-trial activity patterns from large-scale neural recordings. Curr Opin Neurobiol 2007, 17:609-618.
33. Clark D.A., Gabel C.V., Gabel H., Samuel A.D.T. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 2007, 27:6083-6090.
34. Concha M.L., Burdine R.D., Russell C., Schier A.F., Wilson S.W. A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 2000, 28:399-409.
35. Cui G., Jun S.B., Jin X., Pham M.D., Vogel S.S., Lovinger D.M., Costa R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 2013, 494:238-242.
36. deCarvalho T.N., Subedi A., Rock J., Harfe B.D., Thisse C., Thisse B., Halpern M.E., Hong E. Neurotransmitter map of the asymmetric dorsal habenular nuclei of zebrafish. Genesis 2014, 52:636-655.
37. 2+ indicator protein. Eur J Neurosci 2005, 22:627-635.
38. Douglass A.D., Kraves S., Deisseroth K., Schier A.F., Engert F. Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr Biol 2008, 18:1133-1137.
39. Dreosti E., Esposti F., Baden T., Lagnado L. In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat Neurosci 2011, 572:747.
40. Dreosti E., Llopis N.V., Carl M., Yaksi E., Wilson S.W. Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Curr Biol 2014, 24:440-445.
41. Easter S.S., Nicola G.N. The development of vision in the zebrafish (Danio rerio). Dev Biol 1996, 180:646-663.
42. Easter S.S., Nicola G.N. The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol 1997, 31:267-276.
43. Erickson R.P. Stimulus coding in topographic and nontopographic afferent modalities: on the significance of the activity of individual sensory neurons. Psychol Rev 1968, 75:447-465.
44. Euler T., Detwiler P.B., Denk W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 2002, 418:845-852.
45. Faumont S., Rondeau G., Thiele T.R., Lawton K.J., McCormick K.E., Sottile M., Griesbeck O., Heckscher E.S., Roberts W.M., Doe C.Q., Lockery S.R. An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans. PLoS ONE 2011, 6:e24666.
46. Fetcho J.R., McLean D.L. Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications. Ann N Y Acad Sci 2010, 1198:94-104.
47. Friedrich R.W., Jacobson G.A., Zhu P. Circuit neuroscience in zebrafish. Curr Biol 2010, 20:R371-R381.
48. Friedrich R.W., Laurent G. Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 2001, 291:889-894.
49. Gabriel J.P., Ausborn J., Ampatzis K., Mahmood R., Eklöf-Ljunggren E., Manira El A. Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 2011, 14:93-99.
50. Gabriel J.P., Trivedi C.A., Maurer C.M., Ryu S., Bollmann J.H. Layer-specific targeting of direction-selective neurons in the zebrafish optic tectum. Neuron 2012, 76:1147-1160.
51. Georgopoulos A.P., Kalaska J.F., Caminiti R., Massey J.T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 1982, 2:1527-1537.
52. Georgopoulos A.P., Schwartz A.B., Kettner R.E. Neuronal population coding of movement direction. Science 1986, 233:1416-1419.
53. Goldberg M.E., Wurtz R.H. Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. J Neurophysiol 1972, 35:560-574.
54. Goulding M., Lanuza G., Sapir T., Narayan S. The formation of sensorimotor circuits. Curr Opin Neurobiol 2002, 12:508-515.
55. Gray J.M., Hill J.J., Bargmann C.I. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 2005, 102:3184-3191.
56. Grillner S. Megascience efforts and the brain. Neuron 2014, 82:1209-1211.
57. Ha H.-I., Hendricks M., Shen Y., Gabel C.V., Fang-Yen C., Qin Y., Colón-Ramos D., Shen K., Samuel A.D.T., Zhang Y. Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 2010, 68:1173-1186.
58. Harris K.D., Csicsvari J., Hirase H., Dragoi G., Buzsáki G. Organization of cell assemblies in the hippocampus. Nature 2003, 424:552-556.
59. Helmstaedter M., Briggman K.L., Turaga S.C., Jain V., Seung H.S., Denk W. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 2013, 500:168-174.
60. Hendricks M., Jesuthasan S. Asymmetric innervation of the habenula in zebrafish. J Comp Neurol 2007, 502:611-619.
61. Hill D.N., Varga Z., Jia H., Sakmann B., Konnerth A. Multibranch activity in basal and tuft dendrites during firing of layer 5 cortical neurons in vivo. Proc Natl Acad Sci 2013, 110:13618-13623.
62. Hinz F.I., Aizenberg M., Tushev G., Schuman E.M. Protein synthesis-dependent associative long-term memory in larval zebrafish. J Neurosci 2013, 33:15382-15387.
63. Hopp E., Borst A., Haag J. Subcellular mapping of dendritic activity in optic flow processing neurons. J Comp Physiol A 2014, 200:359-370.
64. Huang K.H., Ahrens M.B., Dunn T.W., Engert F. Spinal projection neurons control turning behaviors in zebrafish. Curr Biol 2013, 23:1566-1573.
65. Hubel D.H., Wiesel T.N. Receptive fields of single neurones in the cat's striate cortex. J Physiol 1959, 148:574-591.
66. Hunter P.R., Lowe A.S., Thompson I.D., Meyer M.P. Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity. J Neurosci 2013, 33:13940-13945.
67. Jefferis G.S.X.E., Potter C.J., Chan A.M., Marin E.C., Rohlfing T., Maurer C.R., Luo L. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 2007, 128:1187-1203.
68. Jetti S.K., Vendrell-Llopis N., Yaksi E. Spontaneous activity governs olfactory representations in spatially organized habenular microcircuits. Curr Biol 2014, 24:434-439.
69. Jones L.M., Fontanini A., Sadacca B.F., Miller P., Katz D.B. Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles. Proc Natl Acad Sci 2007, 104:18772-18777.
70. Joshua M., Lisberger S.G. A tale of two species: neural integration in zebrafish and monkeys. Neuroscience 2014, 1-12.
71. Kaufman M.T., Churchland M.M., Ryu S.I., Shenoy K.V. Cortical activity in the null space: permitting preparation without movement. Nat Neurosci 2014, 1-12.
72. Kerlin A.M., Andermann M.L., Berezovskii V.K., Reid R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 2010, 67:858-871.
73. Kettunen P. Advances in experimental medicine and biology 2012, Springer, Dordrecht, Netherlands. M.S. Islam (Ed.).
74. Kinkhabwala A., Riley M., Koyama M., Monen J., Satou C., Kimura Y., Higashijima S.-I., Fetcho J. A structural and functional ground plan for neurons in the hindbrain of zebrafish. Proc Natl Acad Sci 2011, 108:1164-1169.
75. Kohashi T., Oda Y. Initiation of Mauthner- or non-Mauthner-mediated fast escape evoked by different modes of sensory input. J Neurosci 2008, 28:10641-10653.
76. Komiyama T., Sato T.R., O'connor D.H., Zhang Y.-X., Huber D., Hooks B.M., Gabitto M., Svoboda K. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 2010, 464:1182-1186.
77. Koyama M., Kinkhabwala A., Satou C., Higashijima S.-I., Fetcho J. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proc Natl Acad Sci 2011, 108:1170-1175.
78. Krishnan S., Mathuru A.S., Kibat C., Rahman M., Lupton C.E., Stewart J., Claridge-Chang A., Yen S.-C., Jesuthasan S. The right dorsal habenula limits attraction to an odor in zebrafish. Curr Biol 2014, 24:1167-1175.
79. Kuan Y.-S., Gamse J.T., Schreiber A.M., Halpern M.E. Selective asymmetry in a conserved forebrain to midbrain projection. J Exp Zool B Mol Dev Evol 2007, 308:669-678.
80. Kubo F., Hablitzel B., Maschio M.D., Driever W., Baier H., Arrenberg A.B. Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish. Neuron 2014, 81:1344-1359.
81. Larsch J., Ventimiglia D., Bargmann C.I., Albrecht D.R. High-throughput imaging of neuronal activity in Caenorhabditis elegans. Proc Natl Acad Sci 2013, 110:E4266-E4273.
82. Lee A., Mathuru A.S., Teh C., Kibat C., Korzh V., Penney T.B., Jesuthasan S. The habenula prevents helpless behavior in larval zebrafish. Curr Biol 2010, 20:2211-2216.
83. Levoy M., Zhang Z., McDowall I. Recording and controlling the 4D light field in a microscope using microlens arrays. J Microsc 2009, 235:144-162.
84. Lima S.Q., Hromádka T., Znamenskiy P., Zador A.M. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS ONE 2009, 4:e6099.
85. Liu K.S., Fetcho J.R. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 1999, 23:325-335.
86. Livet J., Weissman T.A., Kang H., Draft R.W., Lu J., Bennis R.A., Sanes J.R., Lichtman J.W. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450:56-62.
87. Lu J., Tapia J.C., White O.L., Lichtman J.W. The interscutularis muscle connectome. PLoS Biol 2009, 7:e32.
88. Mank M., Santos A.F., Direnberger S., Mrsic-Flogel T.D., Hofer S.B., Stein V., Hendel T., Reiff D.F., Levelt C., Borst A., Bonhoeffer T., Hübener M., Griesbeck O. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Meth 2008, 5:805-811.
89. Mante V., Sussillo D., Shenoy K.V., Newsome W.T. Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 2013, 503:78-84.
90. Margolis D.J., Lütcke H., Schulz K., Haiss F., Weber B., Kügler S., Hasan M.T., Helmchen F. Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nat Neurosci 2012, 15:1539-1546.
91. Masseck O.A., Hoffmann K.-P. Comparative neurobiology of the optokinetic reflex. Ann N Y Acad Sci 2009, 1164:430-439.
92. McLean D.L., Fan J., Higashijima S.-I., Hale M.E., Fetcho J.R. A topographic map of recruitment in spinal cord. Nature 2007, 446:71-75.
93. McLean D.L., Masino M.A., Koh I.Y.Y., Lindquist W.B., Fetcho J.R. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 2008, 11:1419-1429.
94. Meister M., Lagnado L., Baylor D.A. Concerted signaling by retinal ganglion cells. Science 1995, 270:1207-1210.
95. Meister M., Pine J., Baylor D.A. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 1994, 51:95-106.
96. Miller E.K., Wilson M.A. All my circuits: using multiple electrodes to understand functioning neural networks. Neuron 2008, 60:483-488.
97. Miri A., Daie K., Arrenberg A.B., Baier H., Aksay E., Tank D.W. Spatial gradients and multidimensional dynamics in a neural integrator circuit. Nat Neurosci 2011, 14:1150-1159.
98. Miri A., Daie K., Burdine R.D., Aksay E., Tank D.W. Regression-based identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution. J Neurophysiol 2011, 105:964-980.
99. Miyasaka N., Morimoto K., Tsubokawa T., Higashijima S.-I., Okamoto H., Yoshihara Y. From the olfactory bulb to higher brain centers: genetic visualization of secondary olfactory pathways in zebrafish. J Neurosci 2009, 29:4756-4767.
100. 2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
101. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
102. Mu Y., Li X.-Q., Zhang B., Du J.-L. Visual input modulates audiomotor function via hypothalamic dopaminergic neurons through a cooperative mechanism. Neuron 2012, 75(4):688-699.
103. Muto A., Ohkura M., Abe G., Nakai J., Kawakami K. Real-time visualization of neuronal activity during perception. Curr Biol 2013, 1-5.
104. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 2001, 19:137-141.
105. Naumann E.A., Kampff A.R., Prober D.A., Schier A.F., Engert F. Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 2010, 13:513-520.
106. Neuhauss S.C.F. Behavioral genetic approaches to visual system development and function in zebrafish. J Neurobiol 2003, 54:148-160.
107. Nicolelis M.A., Baccala L.A., Lin R.C., Chapin J.K. Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 1995, 268:1353-1358.
108. Nicolelis M.A., Lin R.C., Woodward D.J., Chapin J.K. Dynamic and distributed properties of many-neuron ensembles in the ventral posterior medial thalamus of awake rats. Proc Natl Acad Sci USA 1993, 90:2212-2216.
109. Nikolaou N., Lowe A.S., Walker A.S., Abbas F., Hunter P.R., Thompson I.D., Meyer M.P. Parametric functional maps of visual inputs to the tectum. Neuron 2012, 76:317-324.
110. O'Shea M., Williams J. The anatomy and output connection of a locust visual interneurone; the lobular giant movement detector (LGMD) neurone. J Comp Physiol 1974, 91:257-266.
111. Odermatt B., Nikolaev A., Lagnado L. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 2012, 73:758-773.
112. Ohki K., Chung S., Ch'ng Y.H., Kara P., Reid R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603.
113. Orger M.B., Kampff A.R., Severi K.E., Bollmann J.H., Engert F. Control of visually guided behavior by distinct populations of spinal projection neurons. Nat Neurosci 2008, 11:327-333.
114. Panier T., Romano S.A., Olive R., Pietri T., Sumbre G., Candelier R., Debrégeas G. Fast functional imaging of multiple brain regions in intact zebrafish larvae using selective plane illumination microscopy. Front Neural Circuits 2013, 7:65.
115. Perkel D.H., Gerstein G.L., Moore G.P. Neuronal spike trains and stochastic point processes. Biophys J 1967, 7:419-440.
116. Peron S.P., Jones P.W., Gabbiani F. Precise subcellular input retinotopy and its computational consequences in an identified visual interneuron. Neuron 2009, 63:830-842.
117. Piggott B.J., Liu J., Feng Z., Wescott S.A., Xu X.Z.S. The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell 2011, 147:922-933.
118. Portugues R., Engert F. The neural basis of visual behaviors in the larval zebrafish. Curr Opin Neurobiol 2009, 19:644-647.
119. Portugues R., Engert F. Adaptive locomotor behavior in larval zebrafish. Front Syst Neurosci 2011, 5:72.
120. Portugues R., Feierstein C.E., Engert F., Orger M.B. Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 2014, 81:1328-1343.
121. Portugues R., Severi K.E., Wyart C., Ahrens M.B. Optogenetics in a transparent animal: circuit function in the larval zebrafish. Curr Opin Neurobiol 2013, 23(1):119-126.
122. Prevedel R., Yoon Y.-G., Hoffmann M., Pak N., Wetzstein G., Kato S., Schrödel T., Raskar R., Zimmer M., Boyden E.S., Vaziri A. Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat Meth 2014, 11:727-730.
123. Renninger S.L., Orger M.B. Two-photon imaging of neural population activity in zebrafish. Methods 2013, 62:255-267.
124. Robles E., Filosa A., Baier H. Precise lamination of retinal axons generates multiple parallel input pathways in the tectum. J Neurosci 2013, 33:5027-5039.
125. Roeser T., Baier H. Visuomotor behaviors in larval zebrafish after GFP-guided laser ablation of the optic tectum. J Neurosci 2003, 23:3726-3734.
126. Ronneberger O., Liu K., Rath M., Rueβ D., Mueller T., Skibbe H., Drayer B., Schmidt T., Filippi A., Nitschke R., Brox T., Burkhardt H., Driever W. ViBE-Z: a framework for 3D virtual colocalization analysis in zebrafish larval brains. Nat Meth 2012, 9:735-742.
127. Sankrithi N., O'Malley D. Activation of a multisensory, multifunctional nucleus in the zebrafish midbrain during diverse locomotor behaviors. Neuroscience 2010, 166:970-993.
128. Satou C., Kimura Y., Hirata H., Suster M.L., Kawakami K., Higashijima S.I. Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons. Development 2013, 140:3927-3931.
129. Schoonheim P.J., Arrenberg A.B., Del Bene F., Baier H. Optogenetic localization and genetic perturbation of saccade-generating neurons in zebrafish. J Neurosci 2010, 30:7111-7120.
130. Schrödel T., Prevedel R., Aumayr K., Zimmer M., Vaziri A. Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light. Nat Meth 2013, 10:1013-1020.
131. Scott E.K., Mason L., Arrenberg A.B., Ziv L., Gosse N.J., Xiao T., Chi N.C., Asakawa K., Kawakami K., Baier H. Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat Meth 2007, 4:323-326.
132. Selverston A.I. Invertebrate central pattern generator circuits. Philos Trans R Soc B 2010, 365:2329-2345.
133. Severi K.E., et al. Neural control and modulation of swimming speed in the larval zebrafish. Neuron 2014, 83:692-707.
134. Shaw B.K., Kristan W.B. The neuronal basis of the behavioral choice between swimming and shortening in the leech: control is not selectively exercised at higher circuit levels. J Neurosci 1997, 17:786-795.
135. Singer W., Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 1995, 18:555-586.
136. 2+ imaging in transgenic mice. J Neurosci 2007, 27:2145-2149.
137. Sompolinsky H. Computational neuroscience: beyond the local circuit. Curr Opin Neurobiol 2014, 1-6.
138. Stuermer C.A. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J Neurosci 1988, 8:4513-4530.
139. Sun X.R., Badura A., Pacheco D.A., Lynch L.A., Schneider E.R., Taylor M.P., Hogue I.B., Enquist L.W., Murthy M., Wang S.S.H. Fast GCaMPs for improved tracking of neuronal activity. Nat Commun 2013, 4:2170.
140. Suster M.L., Abe G., Schouw A., Kawakami K. Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 2011, 6:1998-2021.
141. Suster M.L., Sumiyama K., Kawakami K. Transposon-mediated BAC transgenesis in zebrafish and mice. BMC Genom. 2009, 10:477.
142. Svoboda K., Denk W., Kleinfeld D., Tank D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 1997, 385:161-165.
143. Takemura S.-Y., et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature 2013, 500:175-181.
144. Thestrup T., et al. Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat Meth 2014, 11:175-182.
145. Thiele T.R., et al. Descending control of swim posture by a midbrain nucleus in zebrafish. Neuron 2014, 83:679-691.
146. Trivedi C.A., Bollmann J.H. Visually driven chaining of elementary swim patterns into a goal-directed motor sequence: a virtual reality study of zebrafish prey capture. Front Neural Circuits 2013, 7:86.
147. Tsalik E.L., Hobert O. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J Neurobiol 2003, 56:178-197.
148. Vaadia E., Haalman I., Abeles M., Bergman H., Prut Y., Slovin H., Aertsen A. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 1995, 373:515-518.
149. Valente A., Huang K.H., Portugues R., Engert F. Ontogeny of classical and operant learning behaviors in zebrafish. Learn Mem 2012, 19:170-177.
150. 23 problems in systems neuroscience 2005, Oxford University Press. J. van Hemmen, T. Sejnowski (Eds.).
151. Vladimirov N., Mu Y., Kawashima T., Bennett D.V., Yang C.-T., Looger L.L., Keller P.J., Freeman J., Ahrens M.B. Light-sheet functional imaging in fictively behaving zebrafish. Nat Meth 2014, 1-2.
152. Walls G. The evolutionary history of eye movements. Vis Res 1962, 2:69-80.
153. Wang T.-M., Holzhausen L.C., Kramer R.H. Imaging an optogenetic pH sensor reveals that protons mediate lateral inhibition in the retina. Nat Neurosci 2014, 17:262-268.
154. Wang W.-C., McLean D.L. Selective responses to tonic descending commands by temporal summation in a spinal motor pool. Neuron 2014, 83:708-721.
155. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 1986, 314:1-340.
156. Wyart C., Bene F.D., Warp E., Scott E.K., Trauner D., Baier H., Isacoff E.Y. Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 2009, 461:407-410.
157. Yaksi E., Judkewitz B., Friedrich R.W. Topological reorganization of odor representations in the olfactory bulb. PLoS Biol 2007, 5:e178.
158. Yaksi E., Saint Paul Von F., Niessing J., Bundschuh S.T., Friedrich R.W. Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 2009, 12:474-482.
159. Young M.P., Yamane S. Sparse population coding of faces in the inferotemporal cortex. Science 1992, 256:1327-1331.
160. Zohary E., Shadlen M.N., Newsome W.T. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 1994, 370:140-143.