Miniature microscopes for large-scale imaging of neuronal activity in freely behaving rodents

Current Opinion in Neurobiology

Volumn 32, Issue , 2015, Pages 141-147

  Ziv, Yaniv ^a   Ghosh, Kunal K ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Inscopix Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CALCIUM ION; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; BEHAVIORAL SCIENCE; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; DRUG SCREENING; EMOTIONALITY; FLUORESCENCE IMAGING; HEAD MOVEMENT; HIPPOCAMPUS; HUMAN; IMMOBILIZATION; INTEGRATED MICROSCOPE IMAGING; INTERMETHOD COMPARISON; MICROSCOPE; MICROSCOPY; MINIATURE MICROSCOPE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NERVOUS SYSTEM FUNCTION; NEUROIMAGING; NEUROMONITORING; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; REVIEW; TWO PHOTON MICROSCOPY; ANIMAL; DEVICES; INTRAVITAL MICROSCOPY; NERVE CELL; PHYSIOLOGY; PROCEDURES;

ANIMALS; BEHAVIOR, ANIMAL; INTRAVITAL MICROSCOPY; NEURONS; OPTICAL IMAGING;

EID: 84936943320     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2015.04.001     Document Type: Review

References (61)

1. O'Keefe J.N.L. The Hippocampus as a Cognitive Map 1978, Clarendon.
2. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
3. Buzsaki G. Large-scale recording of neuronal ensembles. Nat Neurosci 2004, 7:446-451.
4. Csicsvari J., Henze D.A., Jamieson B., Harris K.D., Sirota A., Bartho P., Wise K.D., Buzsaki G. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J Neurophysiol 2003, 90:1314-1323.
5. Dupret D., O'Neill J., Pleydell-Bouverie B., Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci 2010, 13:995-1002.
6. Stensola H., Stensola T., Solstad T., Froland K., Moser M.B., Moser E.I. The entorhinal grid map is discretized. Nature 2012, 492:72-78.
7. Panzeri S., Treves A., Schultz S., Rolls E.T. On decoding the responses of a population of neurons from short time windows. Neural Comput 1999, 11:1553-1577.
8. Brown E.N., Frank L.M., Tang D., Quirk M.C., Wilson M.A. A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci: Off J Soc Neurosci 1998, 18:7411-7425.
9. Harris K.D., Csicsvari J., Hirase H., Dragoi G., Buzsaki G. Organization of cell assemblies in the hippocampus. Nature 2003, 424:552-556.
10. Foster D.J., Wilson M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 2006, 440:680-683.
11. Pfeiffer B.E., Foster D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-79.
12. Kentros C. Hippocampal place cells: the "where" of episodic memory?. Hippocampus 2006, 16:743-754.
13. Svoboda K., Denk W., Kleinfeld D., Tank D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 1997, 385:161-165.
14. Sharon D., Grinvald A. Dynamics and constancy in cortical spatiotemporal patterns of orientation processing. Science 2002, 295:512-515.
15. 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.
16. Greenberg D.S., Houweling A.R., Kerr J.N. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci 2008, 11:749-751.
17. Dombeck D.A., Khabbaz A.N., Collman F., Adelman T.L., Tank D.W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 2007, 56:43-57.
18. Scott B.B., Brody C.D., Tank D.W. Cellular resolution functional imaging in behaving rats using voluntary head restraint. Neuron 2013, 80:371-384.
19. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484:62-68.
20. Dombeck D.A., Harvey C.D., Tian L., Looger L.L., Tank D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat Neurosci 2010, 13:1433-1440.
21. Chen J.L., Carta S., Soldado-Magraner J., Schneider B.L., Helmchen F. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 2013, 499:336-340.
22. Helmchen F., Fee M.S., Tank D.W., Denk W. A miniature head-mounted two-photon microscope. high-resolution brain imaging in freely moving animals. Neuron 2001, 31:903-912.
23. Ghosh K.K., Burns L.D., Cocker E.D., Nimmerjahn A., Ziv Y., Gamal A.E., Schnitzer M.J. Miniaturized integration of a fluorescence microscope. Nat Methods 2011, 8:871-878.
24. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci 2013, 16:264-266.
25. Flusberg B.A., Nimmerjahn A., Cocker E.D., Mukamel E.A., Barretto R.P., Ko T.H., Burns L.D., Jung J.C., Schnitzer M.J. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat Methods 2008, 5:935-938.
26. Andermann M.L., Gilfoy N.B., Goldey G.J., Sachdev R.N., Wolfel M., McCormick D.A., Reid R.C., Levene M.J. Chronic cellular imaging of entire cortical columns in awake mice using microprisms. Neuron 2013, 80:900-913.
27. Heys J.G., Rangarajan K.V., Dombeck D.A. The functional micro-organization of grid cells revealed by cellular-resolution imaging. Neuron 2014, 84:1079-1090.
28. Sawinski J., Wallace D.J., Greenberg D.S., Grossmann S., Denk W., Kerr J.N. Visually evoked activity in cortical cells imaged in freely moving animals. Proc Natl Acad Sci USA 2009, 106:19557-19562.
29. Helmchen F., Denk W., Kerr J.N. Miniaturization of two-photon microscopy for imaging in freely moving animals. Cold Spring Harb Protoc 2013, 2013:904-913.
30. Helmchen F., Denk W. Deep tissue two-photon microscopy. Nat Methods 2005, 2:932-940.
31. Wilt B.A., Burns L.D., Wei Ho E.T., Ghosh K.K., Mukamel E.A., Schnitzer M.J. Advances in light microscopy for neuroscience. Annu Rev Neurosci 2009, 32:435-506.
32. Flusberg B.A., Jung J.C., Cocker E.D., Anderson E.P., Schnitzer M.J. In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. Opt Lett 2005, 30:2272-2274.
33. Peters A.J., Chen S.X., Komiyama T. Emergence of reproducible spatiotemporal activity during motor learning. Nature 2014, 510:263-267.
34. Theer P., Hasan M.T., Denk W. Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier. Opt Lett 2003, 28:1022-1024.
35. Mittmann W., Wallace D.J., Czubayko U., Herb J.T., Schaefer A.T., Looger L.L., Denk W., Kerr J.N. Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat Neurosci 2011, 14:1089-1093.
36. Jung J.C., Mehta A.D., Aksay E., Stepnoski R., Schnitzer M.J. In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. J Neurophysiol 2004, 92:3121-3133.
37. Barretto R.P., Messerschmidt B., Schnitzer M.J. In vivo fluorescence imaging with high-resolution microlenses. Nat Methods 2009, 6:511-512.
38. Barretto R.P., Ko T.H., Jung J.C., Wang T.J., Capps G., Waters A.C., Ziv Y., Attardo A., Recht L., Schnitzer M.J. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nat Med 2011, 17:223-228.
39. Grewe B.F., Lecoq J., Li L.K., Marshall J., Venkataraman J., Grundemann J., Luthi A.A. Calcium imaging of stimulus specific neuronal responses in the lateral amygdala during fear learning. Society for Neuroscience Annual Meeting 2014.
40. Parker J.G., Marshall J.D., Ahanonu B., Grewe B., Zhong Li J., Ehlers M.D., Schnitzer M.J. Parallel remodeling of direct and indirect pathway neuronal activity in the nucleus accumbens during Pavlovian reward conditioning. Society for Neuroscience Annual Meeting 2014.
41. Jennings J.H., Ung R.L., Resendez S.L., Stamatakis A.M., Taylor J.G., Huang J., Veleta K., Kantak P.A., Aita M., Shilling-Scrivo K., et al. Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 2015, 160:516-527.
42. Sheffield M.E., Dombeck D.A. Calcium transient prevalence across the dendritic arbour predicts place field properties. Nature 2015, 517:200-204.
43. Grewe B.F., Langer D., Kasper H., Kampa B.M., Helmchen F. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat Methods 2010, 7:399-405.
44. Ravassard P., Kees A., Willers B., Ho D., Aharoni D., Cushman J., Aghajan Z.M., Mehta M.R. Multisensory control of hippocampal spatiotemporal selectivity. Science 2013, 340:1342-1346.
45. Aghajan Z.M., Acharya L., Moore J.J., Cushman J.D., Vuong C., Mehta M.R. Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. Nat Neurosci 2015, 18:121-128.
46. Denk W., Svoboda K. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 1997, 18:351-357.
47. Mukamel E.A., Nimmerjahn A., Schnitzer M.J. Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 2009, 63:747-760.
48. 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., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
49. Lever C., Wills T., Cacucci F., Burgess N., O'Keefe J. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 2002, 416:90-94.
50. O'Keefe J., Speakman A. Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 1987, 68:1-27.
51. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 2009, 6:875-881.
52. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13:1161-1169.
53. Youmans K.L., Tai L.M., Nwabuisi-Heath E., Jungbauer L., Kanekiyo T., Gan M., Kim J., Eimer W.A., Estus S., Rebeck G.W., et al. APOE4-specific changes in Abeta accumulation in a new transgenic mouse model of Alzheimer disease. J Biol Chem 2012, 287:41774-41786.
54. Sterniczuk R., Antle M.C., Laferla F.M., Dyck R.H. Characterization of the 3×Tg-AD mouse model of Alzheimer's disease: part 2. Behavioral and cognitive changes. Brain Res 2010, 1348:149-155.
55. Filali M., Lalonde R., Theriault P., Julien C., Calon F., Planel E. Cognitive and non-cognitive behaviors in the triple transgenic mouse model of Alzheimer's disease expressing mutated APP, PS1, and Mapt (3×Tg-AD). Behav Brain Res 2012, 234:334-342.
56. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc Natl Acad Sci USA 2004, 101:13363-13367.
57. Knowles J.K., Rajadas J., Nguyen T.V., Yang T., LeMieux M.C., Vander Griend L., Ishikawa C., Massa S.M., Wyss-Coray T., Longo F.M. The p75 neurotrophin receptor promotes amyloid-beta(1-42)-induced neuritic dystrophy in vitro and in vivo. J Neurosci 2009, 29:10627-10637.
58. Karran E., Mercken M., De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov 2011, 10:698-712.
59. Busche M.A., Chen X., Henning H.A., Reichwald J., Staufenbiel M., Sakmann B., Konnerth A. Critical role of soluble amyloid-beta for early hippocampal hyperactivity in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2012, 109:8740-8745.
60. Cacucci F., Yi M., Wills T.J., Chapman P., O'Keefe J. Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model. Proc Natl Acad Sci USA 2008, 105:7863-7868.
61. Berdyyeva T., Otte S., Aluisio L., Ziv Y., Burns L.D., Dugovic C., Yun S., Ghosh K.K., Schnitzer M.J., Lovenberg T., et al. Zolpidem reduces hippocampal neuronal activity in freely behaving mice: a large scale calcium imaging study with miniaturized fluorescence microscope. PLoS One 2014, 9:e112068.