Tools for probing local circuits: High-density silicon probes combined with optogenetics

Neuron

Volumn 86, Issue 1, 2015, Pages 92-105

  Buzsáki, György ^a   Stark, Eran ^a   Berényi, Antal ^a,b   Khodagholy, Dion ^a   Kipke, Daryl R ^c   Yoon, Euisik ^d   Wise, Kensall D ^d  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SZEGED   (Hungary)

^c NeuroNexus Technologies Inc ^*  (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SILICON;

ACTION POTENTIAL; ALGORITHM; AMPLIFIER; DATA PROCESSING; ELECTRODE; ELECTRONICS; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; INFORMATION PROCESSING DEVICE; LOCAL FIELD POTENTIAL; MICROELECTROMECHANICAL SYSTEM; MICROMANIPULATOR; NEUROPHYSIOLOGY; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; REVIEW; SIGNAL NOISE RATIO; SILICON PROBE; TELEMETRY; ANIMAL; CHEMISTRY; DEVICES; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; ANIMALS; ELECTROPHYSIOLOGY; NERVE NET; NEURONS; OPTOGENETICS; SILICON;

EID: 84930369995     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.01.028     Document Type: Review

References (171)

1. Abidian M.R., Martin D.C. Experimental and theoretical characterization of implantable neural microelectrodes modified with conducting polymer nanotubes. Biomaterials 2008, 29:1273-1283.
2. Adrian E.D., Moruzzi G. Impulses in the pyramidal tract. J.Physiol. 1939, 97:153-199.
3. Agarwal G., Stevenson I.H., Berényi A., Mizuseki K., Buzsáki G., Sommer F.T. Spatially distributed local fields in the hippocampus encode rat position. Science 2014, 344:626-630.
4. Al-Ashmouny K.M., Chang S.I., Yoon E. A 4 muW/Ch analog front-end module with moderate inversion and power-scalable sampling operation for 3-D neural microsystems. IEEE Trans. Biomed. Circuits Syst. 2012, 6:403-413.
5. Alivisatos A.P., Chun M., Church G.M., Deisseroth K., Donoghue J.P., Greenspan R.J., McEuen P.L., Roukes M.L., Sejnowski T.J., Weiss P.S., Yuste R. Neuroscience. The brain activity map. Science 2013, 339:1284-1285.
6. Alonso M., Lepousez G., Sebastien W., Bardy C., Gabellec M.M., Torquet N., Lledo P.M. Activation of adult-born neurons facilitates learning and memory. Nat. Neurosci. 2012, 15:897-904.
7. Ascoli G.A., Alonso-Nanclares L., Anderson S.A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzsáki G., Cauli B., Defelipe J., Fairén A., et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 2008, 9:557-568. Petilla Interneuron Nomenclature Group.
8. Bai Q., Wise K.D. Single-unit neural recording with active microelectrode arrays. IEEE Trans. Biomed. Eng. 2001, 48:911-920.
9. Bai Q., Wise K.D., Anderson D.J. A high-yield microassembly structure for three-dimensional microelectrode arrays. IEEE Trans. Biomed. Eng. 2000, 47:281-289.
10. Bartels J., Andreasen D., Ehirim P., Mao H., Seibert S., Wright E.J., Kennedy P. Neurotrophic electrode: method of assembly and implantation into human motor speech cortex. J.Neurosci. Methods 2008, 174:168-176.
11. Barthó P., Hirase H., Monconduit L., Zugaro M., Harris K.D., Buzsáki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J.Neurophysiol. 2004, 92:600-608.
12. Berényi A., Belluscio M., Mao D., Buzsáki G. Closed-loop control of epilepsy by transcranial electrical stimulation. Science 2012, 337:735-737.
13. Berényi A., Somogyvári Z., Nagy A.J., Roux L., Long J.D., Fujisawa S., Stark E., Leonardo A., Harris T.D., Buzsáki G. Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. J.Neurophysiol. 2014, 111:1132-1149.
14. Berndt A., Schoenenberger P., Mattis J., Tye K.M., Deisseroth K., Hegemann P., Oertner T.G. High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 2011, 108:7595-7600.
15. Bjornsson C.S., Oh S.J., Al-Kofahi Y.A., Lim Y.J., Smith K.L., Turner J.N., De S., Roysam B., Shain W., Kim S.J. Effects of insertion conditions on tissue strain and vascular damage during neuroprosthetic device insertion. J.Neural Eng. 2006, 3:196-207.
16. Blanche T.J., Spacek M.A., Hetke J.F., Swindale N.V. Polytrodes: high-density silicon electrode arrays for large-scale multiunit recording. J.Neurophysiol. 2005, 93:2987-3000.
17. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
18. Broome B.M., Jayaraman V., Laurent G. Encoding and decoding of overlapping odor sequences. Neuron 2006, 51:467-482.
19. Brown M.T., Tan K.R., O'Connor E.C., Nikonenko I., Muller D., Lüscher C. Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 2012, 492:452-456.
20. Buzsáki G. Large-scale recording of neuronal ensembles. Nat. Neurosci. 2004, 7:446-451.
21. Buzsáki G., Mizuseki K. The log-dynamic brain: how skewed distributions affect network operations. Nat. Rev. Neurosci. 2014, 15:264-278.
22. Buzsáki G., Penttonen M., Nádasdy Z., Bragin A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus invivo. Proc. Natl. Acad. Sci. USA 1996, 93:9921-9925.
23. Buzsáki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012, 13:407-420.
24. Buzsáki G., Logothetis N., Singer W. Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron 2013, 80:751-764.
25. Carandini M. From circuits to behavior: a bridge too far?. Nat. Neurosci. 2012, 15:507-509.
26. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
27. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Targeted optogenetic stimulation and recording of neurons invivo using cell-type-specific expression of Channelrhodopsin-2. Nat. Protoc. 2010, 5:247-254.
28. Carlén M., Meletis K., Siegle J.H., Cardin J.A., Futai K., Vierling-Claassen D., Rühlmann C., Jones S.R., Deisseroth K., Sheng M., et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol. Psychiatry 2012, 17:537-548.
29. Cavanaugh J., Monosov I.E., McAlonan K., Berman R., Smith M.K., Cao V., Wang K.H., Boyden E.S., Wurtz R.H. Optogenetic inactivation modifies monkey visuomotor behavior. Neuron 2012, 76:901-907.
30. Chen J., Wise K.D., Hetke J.F., Bledsoe S.C. A multichannel neural probe for selective chemical delivery at the cellular level. IEEE Trans. Biomed. Eng. 1997, 44:760-769.
31. Chestek C.A., Gilja V., Nuyujukian P., Foster J.D., Fan J.M., Kaufman M.T., Churchland M.M., Rivera-Alvidrez Z., Cunningham J.P., Ryu S.I., Shenoy K.V. Long-term stability of neural prosthetic control signals from silicon cortical arrays in rhesus macaque motor cortex. J.Neural Eng. 2011, 8:045005.
32. Cheung K.C., Djupsund K., Yang D., Lee L.P. Implantable multichannel electrode array based on SOI technology. J.Microelectromech Syst. 2003, 12:179-184.
33. Chichilnisky E.J., Baylor D.A. Receptive-field microstructure of blue-yellow ganglion cells in primate retina. Nat. Neurosci. 1999, 2:889-893.
34. Chuong A.S., Miri M.L., Busskamp V., Matthews G.A., Acker L.C., Sørensen A.T., Young A., Klapoetke N.C., Henninger M.A., Kodandaramaiah S.B., et al. Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nat. Neurosci. 2014, 17:1123-1129.
35. Claverol-Tinture E., Nadasdy Z. Intersection of microwire electrodes with proximal CA1 stratum-pyramidale neurons at insertion for multiunit recordings predicted by a 3-D computer model. IEEE Trans. Biomed. Eng. 2004, 51:2211-2216.
36. Csicsvari J., Hirase H., Czurko A., Buzsáki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 1998, 21:179-189.
37. Csicsvari J., Henze D.A., Jamieson B., Harris K.D., Sirota A., Barthó P., Wise K.D., Buzsáki G. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J.Neurophysiol. 2003, 90:1314-1323.
38. de Lecea L., Huerta R. Hypocretin (orexin) regulation of sleep-to-wake transitions. Front. Pharmacol. 2014, 5:16.
39. Deisseroth K. Optogenetics. Nat. Methods 2011, 8:26-29.
40. Diester I., Kaufman M.T., Mogri M., Pashaie R., Goo W., Yizhar O., Ramakrishnan C., Deisseroth K., Shenoy K.V. An optogenetic toolbox designed for primates. Nat. Neurosci. 2011, 14:387-397.
41. Drake K.L., Wise K.D., Farraye J., Anderson D.J., BeMent S.L. Performance of planar multisite microprobes in recording extracellular single-unit intracortical activity. IEEE Trans. Biomed. Eng. 1988, 35:719-732.
42. Du J., Riedel-Kruse I.H., Nawroth J.C., Roukes M.L., Laurent G., Masmanidis S.C. High-resolution three-dimensional extracellular recording of neuronal activity with microfabricated electrode arrays. J.Neurophysiol. 2009, 101:1671-1678.
43. Du J., Blanche T.J., Harrison R.R., Lester H.A., Masmanidis S.C. Multiplexed, high density electrophysiology with nanofabricated neural probes. PLoS ONE 2011, 6:e26204.
44. Einevoll G.T., Franke F., Hagen E., Pouzat C., Harris K.D. Towards reliable spike-train recordings from thousands of neurons with multielectrodes. Curr. Opin. Neurobiol. 2012, 22:11-17.
45. Einevoll G.T., Kayser C., Logothetis N.K., Panzeri S. Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat. Rev. Neurosci. 2013, 14:770-785.
46. Fee M.S., Leonardo A. Miniature motorized microdrive andcommutator system for chronic neural recording in small animals. J.Neurosci. Methods 2001, 112:83-94.
47. Fujisawa S., Amarasingham A., Harrison M.T., Buzsáki G. Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat. Neurosci. 2008, 11:823-833.
48. Gerits A., Farivar R., Rosen B.R., Wald L.L., Boyden E.S., Vanduffel W. Optogenetically induced behavioral and functional network changes in primates. Curr. Biol. 2012, 22:1722-1726.
49. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., Diester I., Goshen I., Thompson K.R., Deisseroth K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141:154-165.
50. Gray C.M., Goodell B., Lear A. Multichannel micromanipulator and chamber system for recording multineuronal activity in alert, non-human primates. J.Neurophysiol. 2007, 98:527-536.
51. Greenwald E., Mollazadeh M., Hu C., Wei T., Culurciello E., Thakor V. A VLSI neural monitoring system with ultra-wideband telemetry for awake behaving subjects. IEEE Trans. Biomed. Circ. Syst. 2011, 5:112-119.
52. Grienberger C., Konnerth A. Imaging calcium in neurons. Neuron 2012, 73:862-885.
53. Gunaydin L.A., Yizhar O., Berndt A., Sohal V.S., Deisseroth K., Hegemann P. Ultrafast optogenetic control. Nat. Neurosci. 2010, 13:387-392.
54. Halassa M.M., Siegle J.H., Ritt J.T., Ting J.T., Feng G., Moore C.I. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat. Neurosci. 2011, 14:1118-1120.
55. Han X., Qian X., Bernstein J.G., Zhou H.H., Franzesi G.T., Stern P., Bronson R.T., Graybiel A.M., Desimone R., Boyden E.S. Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain. Neuron 2009, 62:191-198.
56. Harris K.D., Henze D.A., Csicsvari J., Hirase H., Buzsáki G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J.Neurophysiol. 2000, 84:401-414.
57. Harrison R.R. The design of integrated circuits to observe brain activity. Proc. IEEE 2008, 96:1203-1216.
58. Harrison R.R., Fotowat H., Chan R., Kier R.J., Olberg R., Leonardo A., Gabbiani F. Wireless neural/emg telemetry systems for small freely moving animals. IEEE Trans. Biomed. Circ. Syst. 2011, 5:103-111.
59. Haubensak W., Kunwar P.S., Cai H., Ciocchi S., Wall N.R., Ponnusamy R., Biag J., Dong H.W., Deisseroth K., Callaway E.M., et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010, 468:270-276.
60. Henze D.A., Borhegyi Z., Csicsvari J., Mamiya A., Harris K.D., Buzsáki G. Intracellular features predicted by extracellular recordings in the hippocampus invivo. J.Neurophysiol. 2000, 84:390-400.
61. Hofmann U.G., Folkers A., Mösch F., Malina T., Menne K.M., Biella G., Fagerstedt P., De Schutter E., Jensen W., Yoshida K., et al. A novel high channel-count system for acute multisite neuronal recordings. IEEE Trans. Biomed. Eng. 2006, 53:1672-1677.
62. Hoogerwerf A.C., Wise K.D. A three-dimensional microelectrode array for chronic neural recording. IEEE Trans. Biomed. Eng. 1994, 41:1136-1146.
63. Huber D., Petreanu L., Ghitani N., Ranade S., Hromádka T., Mainen Z., Svoboda K. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 2008, 451:61-64.
64. Hutzler M., Fromherz P. Silicon chip with capacitors and transistors for interfacing organotypic brain slice of rat hippocampus. Eur. J. Neurosci. 2004, 19:2231-2238.
65. Im M., Cho I.-J., Wu F., Wise K.D., Yoon E. Neural probes integrated with optical mixer/splitter waveguides and multiple stimulation sites. Conf. Proc. IEEE Micro Electro. Mech. Sys. 2011, 1051-1053.
66. Jackson A., Fetz E.E. Compact movable microwire array for long-term chronic unit recording in cerebral cortex of primates. J.Neurophysiol. 2007, 98:3109-3118.
67. Jamille F.H., David J.A. Silicon microelectrodes for extracellular recording. Handbook of Neuroprosthetic Methods 2002, CRC Press, London.
68. Jefferys J.G. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol. Rev. 1995, 75:689-723.
69. Khodagholy D., Doublet T., Gurfinkel M., Quilichini P., Ismailova E., Leleux P., Herve T., Sanaur S., Bernard C., Malliaras G.G. Highly conformable conducting polymer electrodes for invivo recordings. Adv. Mater. 2011, 23:H268-H272.
70. Khodagholy D., Gelinas J.N., Thesen T., Doyle W., Devinsky O., Malliaras G.G., Buzsáki G. NeuroGrid: recording action potentials from the surface of the brain. Nat. Neurosci. 2015, 18. 310-315.
71. Kim D.H., Viventi J., Amsden J.J., Xiao J., Vigeland L., Kim Y.S., Blanco J.A., Panilaitis B., Frechette E.S., Contreras D., et al. Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat. Mater. 2010, 9:511-517.
72. Kim T.I., McCall J.G., Jung Y.H., Huang X., Siuda E.R., Li Y., Song J., Song Y.M., Pao H.A., Kim R.H., et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 2013, 340:211-216.
73. Kipke D.R., Vetter R.J., Williams J.C., Hetke J.F. Silicon-substrate intracortical microelectrode arrays for long-term recording of neuronal spike activity in cerebral cortex. IEEE Trans. Neural Syst. Rehab. Eng. 2003, 11:151-155.
74. Kipke D.R., Shain W., Buzsáki G., Fetz E., Henderson J.M., Hetke J.F., Schalk G. Advanced neurotechnologies for chronic neural interfaces: new horizons and clinical opportunities. J.Neurosci. 2008, 28:11830-11838.
75. Klapoetke N.C., Murata Y., Kim S.S., Pulver S.R., Birdsey-Benson A., Cho Y.K., Morimoto T.K., Chuong A.S., Carpenter E.J., Tian Z., et al. Independent optical excitation of distinct neural populations. Nat. Methods 2014, 11:338-346.
76. Kozai T.D., Marzullo T.C., Hooi F., Langhals N.B., Majewska A.K., Brown E.B., Kipke D.R. Reduction of neurovascular damage resulting from microelectrode insertion into the cerebral cortex using invivo two-photon mapping. J.Neural Eng. 2010, 7:046011.
77. Kozai T.D., Langhals N.B., Patel P.R., Deng X., Zhang H., Smith K.L., Lahann J., Kotov N.A., Kipke D.R. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat. Mater. 2012, 11:1065-1073.
78. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
79. Krook-Magnuson E., Armstrong C., Oijala M., Soltesz I. On-demandoptogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat. Comm. 2013, 4:1376.
80. Kvitsiani D., Ranade S., Hangya B., Taniguchi H., Huang J.Z., Kepecs A. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 2013, 498:363-366.
81. Lee S.H., Kwan A.C., Zhang S., Phoumthipphavong V., Flannery J.G., Masmanidis S.C., Taniguchi H., Huang Z.J., Zhang F., Boyden E.S., et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 2012, 488:379-383.
82. Lei N., Ramakrishnan S., Shi P., Orcutt J.S., Yuste R., Kam L.C., Shepard K.L. High-resolution extracellular stimulation of dispersed hippocampal culture with high-density CMOS multielectrode array based on non-Faradaic electrodes. J.Neural Eng. 2011, 8:044003.
83. Li Y., Baek K., Gulari M., Wise K.D. A drug-delivery probe with an in-line flowmeter based on trench refill and chemical mechanical polishing techniques 2007, 1144-1147. IEEE Sensors.
84. Lin J.Y., Lin M.Z., Steinbach P., Tsien R.Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 2009, 96:1803-1814.
85. Lin C.P., Chen Y.P., Hung C.P. Tuning and spontaneous spike time synchrony share a common structure in macaque inferior temporal cortex. J.Neurophysiol. 2014, 112:856-869.
86. Logothetis N.K. The underpinnings of the BOLD functional magnetic resonance imaging signal. J.Neurosci. 2003, 23:3963-3971.
87. Lu Y., Li Y., Pan J., Wei P., Liu N., Wu B., Cheng J., Lu C., Wang L. Poly(3,4-ethylenedioxythiophene)/poly(styrenesulfonate)-poly(vinyl alcohol)/poly(acrylic acid) interpenetrating polymer networks for improving optrode-neural tissue interface in optogenetics. Biomaterials 2012, 33:378-394.
88. Ludwig K.A., Uram J.D., Yang J., Martin D.C., Kipke D.R. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film. J.Neural Eng. 2006, 3:59-70.
89. Madisen L., Mao T., Koch H., Zhuo J.M., Berenyi A., Fujisawa S., Hsu Y.W., Garcia A.J., Gu X., Zanella S., et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 2012, 15:793-802.
90. Marblestone A.H., Zamft B.M., Maguire Y.G., Shapiro M.G., Cybulski T.R., Glaser J.I., Amodei D., Stranges P.B., Kalhor R., Dalrymple D.A., et al. Physical principles for scalable neural recording. Front. Comp. Neurosci. 2013, 7:137.
91. McCreery D., Lossinsky A., Pikov V., Liu X. Microelectrode array for chronic deep-brain microstimulation and recording. IEEE Trans. Biomed. Eng. 2006, 53:726-737.
92. McNaughton B.L., O'Keefe J., Barnes C.A. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J.Neurosci. Methods 1983, 8:391-397.
93. Meister M., Pine J., Baylor D.A. Multi-neuronal signals from the retina: acquisition and analysis. J.Neurosci. Methods 1994, 51:95-106.
94. Miesenböck G. The optogenetic catechism. Science 2009, 326:395-399.
95. Miles R. Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig invitro. J.Physiol. 1990, 428:61-77.
96. Mizuseki K., Diba K., Pastalkova E., Teeters J., Sirota A., Buzsáki G. Neurosharing: large-scale data sets (spike, LFP) recorded from the hippocampal-entorhinal system in behaving rats. F1000Research 2014, 3:98.
97. Moffitt M.A., McIntyre C.C. Model-based analysis of cortical recording with silicon microelectrodes. Clin. Neurophys. 2005, 116:2240-2250.
98. Montgomery S.M., Sirota A., Buzsáki G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J.Neurosci. 2008, 28:6731-6741.
99. Moore A.K., Wehr M. Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J.Neurosci. 2013, 33:13713-13723.
100. Motta P.S., Judy J.W. Multielectrode microprobes for deep-brain stimulation fabricated with a customizable 3-D electroplating process. IEEE Trans. Biomed. Eng. 2005, 52:923-933.
101. Muller J., Bakkum D.J., Hierlemann A. Sub-millisecond closed-loop feedback stimulation between arbitrary sets of individual neurons. Front. Neural Circ. 2012, 6:121.
102. Musallam S., Bak M.J., Troyk P.R., Andersen R.A. A floating metal microelectrode array for chronic implantation. J.Neurosci. Methods 2007, 160:122-127.
103. Nádasdy Z., Csicsvári J., Penttonen M., Hetke J., Wise K., Buzsáki G. Extracellular recording and analysis of neuronal activity: from single cells to ensembles. Neuronal Ensembles: Strategies for Recording and Decoding 1998, Wiley, New York. H.B. Eichenbaum, J.L. Davis (Eds.).
104. Najafi K., Wise K.D. An implantable multielectrode array with on-chip signal-processing. IEEE J. Solid-State Circ. 1986, 21:1035-1044.
105. Neves H.P., Ruther P. The NeuroProbes Project. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 2007:6443-6445.
106. Nicolelis M.A., Ghazanfar A.A., Faggin B.M., Votaw S., Oliveira L.M. Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron 1997, 18:529-537.
107. Nordhausen C.T., Maynard E.M., Normann R.A. Single unit recording capabilities of a 100 microelectrode array. Brain Res. 1996, 726:129-140.
108. Olsson R.H., Buhl D.L., Sirota A.M., Buzsáki G., Wise K.D. Band-tunable and multiplexed integrated circuits for simultaneous recording and stimulation with microelectrode arrays. IEEE Trans. Biomed. Eng. 2005, 52:1303-1311.
109. Packer A.M., Roska B., Häusser M. Targeting neurons and photons for optogenetics. Nat. Neurosci. 2013, 16:805-815.
110. Pang C., Cham J., Nenadic Z., Musallam S., Tai Y.C., Burdick J., Andersen R. A new multi-site probe array with monolithically integrated parylene flexible cable for neural prostheses. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2005, 7:7114-7117.
111. Paz J.T., Davidson T.J., Frechette E.S., Delord B., Parada I., Peng K., Deisseroth K., Huguenard J.R. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 2013, 16:64-70.
112. Perlin G., Wise K. The effect of the substrate on the extracellular neural activity recorded micromachined silicon microprobes. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2004, 3:2002-2005.
113. Perlin G.E., Wise K.D. An ultra compact integrated front end for wireless neural recording microsystems. J.Microelectromech. Syst. 2010, 19:1409-1421.
114. Pi H.J., Hangya B., Kvitsiani D., Sanders J.I., Huang Z.J., Kepecs A. Cortical interneurons that specialize in disinhibitory control. Nature 2013, 503:521-524.
115. Polikov V.S., Tresco P.A., Reichert W.M. Response of brain tissue to chronically implanted neural electrodes. J.Neurosci. Methods 2005, 148:1-18.
116. Pouzat C., Mazor O., Laurent G. Using noise signature to optimize spike-sorting and to assess neuronal classification quality. J.Neurosci. Methods 2002, 122:43-57.
117. Ramirez S., Liu X., Lin P.A., Suh J., Pignatelli M., Redondo R.L., Ryan T.J., Tonegawa S. Creating a false memory in the hippocampus. Science 2013, 341:387-391.
118. Reimann M.W., Anastassiou C.A., Perin R., Hill S.L., Markram H., Koch C. A biophysically detailed model of neocortical local field potentials predicts the critical role of active membrane currents. Neuron 2013, 79:375-390.
119. Rennaker R.L., Ruyle A.M., Street S.E., Sloan A.M. An economical multi-channel cortical electrode array for extended periods of recording during behavior. J.Neurosci. Methods 2005, 142:97-105.
120. Riera J.J., Ogawa T., Goto T., Sumiyoshi A., Nonaka H., Evans A., Miyakawa H., Kawashima R. Pitfalls in the dipolar model for the neocortical EEG sources. J.Neurophysiol. 2012, 108:956-975.
121. Rousche P.J., Normann R.A. Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex. J.Neurosci. Methods 1998, 82:1-15.
122. Roux L., Buzsáki G. Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology 2015, 88:10-23.
123. Roux L., Stark E., Sjulson L., Buzsáki G. Invivo optogenetic identification and manipulation of GABAergic interneuron subtypes. Curr. Opin. Neurobiol. 2014, 26:88-95.
124. Royer S., Zemelman B.V., Barbic M., Losonczy A., Buzsáki G., Magee J.C. Multi-array silicon probes with integrated optical fibers: light-assistedperturbation and recording of local neural circuits in the behaving animal. Eur. J. Neurosci. 2010, 31:2279-2291.
125. Royer S., Zemelman B.V., Losonczy A., Kim J., Chance F., Magee J.C., Buzsáki G. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 2012, 15:769-775.
126. Rubehn B., Wolff S.B., Tovote P., Lüthi A., Stieglitz T. A polymer-based neural microimplant for optogenetic applications: design and first invivo study. Lab Chip 2013, 13:579-588.
127. Ruther P., Holzhammer T., Herwik S., Rich P.D., Dalley J.W., Paul O., Holtzman T. Compact wireless neural recording system for small animals using silicon-based probe arrays. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011, 2011:2284-2287.
128. Scanziani M., Häusser M. Electrophysiology in the age of light. Nature 2009, 461:930-939.
129. Schomburg E.W., Anastassiou C.A., Buzsáki G., Koch C. The spiking component of oscillatory extracellular potentials in the rat hippocampus. J.Neurosci. 2012, 32:11798-11811.
130. Schwarz D.A., Lebedev M.A., Hanson T.L., Dimitrov D.F., Lehew G., Meloy J., Rajangam S., Subramanian V., Ifft P.J., Li Z., et al. Chronic, wireless recordings of large-scale brain activity in freely moving rhesus monkeys. Nat. Methods. 2014, 11:670-676.
131. Schwindel C.D., Ali K., McNaughton B.L., Tatsuno M. Long-term recordings improve the detection of weak excitatory-excitatory connections in rat prefrontal cortex. J.Neurosci. 2014, 34:5454-5467.
132. Scott K.M., Du J., Lester H.A., Masmanidis S.C. Variability of acute extracellular action potential measurements with multisite silicon probes. J.Neurosci. Methods 2012, 211:22-30.
133. Seidl K., Spieth S., Herwik S., Steigert J., Zengerle R., Paul O., Ruther P. In-plane silicon probes for simultaneous neural recording and drug delivery. J.Micromech. Microeng. 2010, 20:105006.
134. Seidl K., Herwik S., Torfs T., Neves H.P., Paul O., Ruther P. CMOS-based high-density silicon microprobe arrays for electronic depth control in intracortical neural recording. J.Microelectromech. Syst. 2011, 20:1439-1448.
135. Seymour J.P., Kipke D.R. Neural probe design for reduced tissue encapsulation in CNS. Biomaterials 2007, 28:3594-3607.
136. Seymour J.P., Langhals N.B., Anderson D.J., Kipke D.R. Novel multi-sided, microelectrode arrays for implantable neural applications. Biomed. Microdevices 2011, 13:441-451.
137. Shain W., Spataro L., Dilgen J., Haverstick K., Retterer S., Isaacson M., Saltzman M., Turner J.N. Controlling cellular reactive responses around neural prosthetic devices using peripheral and local intervention strategies. IEEE Trans. Neural Syst. Rehab. Eng. 2003, 11:186-188.
138. Shoham S., O'Connor D.H., Segev R. How silent is the brain: is there a "dark matter" problem in neuroscience?. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2006, 192:777-784.
139. Sodagar A.M., Wise K.D., Najafi K. A fully integrated mixed-signal neural processor for implantable multichannel cortical recording. IEEE Trans. Biomed. Eng. 2007, 54:1075-1088.
140. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
141. Spataro L., Dilgen J., Retterer S., Spence A.J., Isaacson M., Turner J.N., Shain W. Dexamethasone treatment reduces astroglia responses to inserted neuroprosthetic devices in rat neocortex. Exp. Neurol. 2005, 194:289-300.
142. Stark E., Koos T., Buzsáki G. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J.Neurophysiol. 2012, 108:349-363.
143. Stark E., Eichler R., Roux L., Fujisawa S., Rotstein H.G., Buzsáki G. Inhibition-induced theta resonance in cortical circuits. Neuron 2013, 80:1263-1276.
144. Stark E., Roux L., Eichler R., Senzai Y., Royer S., Buzsáki G. Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 2014, 83:467-480.
145. Stevenson I.H., Kording K.P. How advances in neural recording affect data analysis. Nat. Neurosci. 2011, 14:139-142.
146. Stieglitz T., Schuettler M., Koch K.P. Implantable biomedical microsystems for neural prostheses. IEE Eng. Med. Biol. Mag. 2005, 24:58-65.
147. Suner S., Fellows M.R., Vargas-Irwin C., Nakata G.K., Donoghue J.P. Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex. IEEE Trans. Neural Syst. Rehab. Eng. 2005, 13:524-541.
148. Szuts T.A., Fadeyev V., Kachiguine S., Sher A., Grivich M.V., Agrochão M., Hottowy P., Dabrowski W., Lubenov E.V., Siapas A.G., et al. A wireless multi-channel neural amplifier for freely moving animals. Nat. Neurosci. 2011, 14:263-269.
149. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
150. Tien L.W., Wu F., Tang-Schomer M.D., Yoon E., Omenetto F.G., Kaplan D.L. Silk as a multifunctional biomaterial substrate for reduced glial scarring around brain-penetrating electrodes. Adv. Funct. Mater. 2013, 23:3185-3193.
151. Tsai P.S., Kaufhold J.P., Blinder P., Friedman B., Drew P.J., Karten H.J., Lyden P.D., Kleinfeld D. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J.Neurosci. 2009, 29:14553-14570.
152. Vandecasteele M., M.S., Royer S., Belluscio M., Berenyi A., Diba K., Fujisawa S., Grosmark A., Mao D., Mizuseki K., et al. Large-scale recording of neurons by movable silicon probes in behaving rodents. JoVE 2012, e3568.
153. Viventi J., Kim D.H., Vigeland L., Frechette E.S., Blanco J.A., Kim Y.S., Avrin A.E., Tiruvadi V.R., Hwang S.W., Vanleer A.C., et al. Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity invivo. Nat. Neurosci. 2011, 14:1599-1605.
154. Voigts J., Siegle J.H., Pritchett D.L., Moore C.I. The flexDrive: an ultra-light implant for optical control and highly parallel chronic recording of neuronal ensembles in freely moving mice. Front. Syst. Neurosci. 2013, 7:8.
155. Wentz C.T., Bernstein J.G., Monahan P., Guerra A., Rodriguez A., Boyden E.S. A wirelessly powered and controlled device for optical neural control of freely-behaving animals. J.Neural Eng. 2011, 8:046021.
156. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
157. Wise K.D., Anderson D.J., Hetke J.F., Kipke D.R., Najafi K. Wireless implantable microsystems: high-density electronic interfaces to the nervous system. Proc. IEEE 2004, 92:76-97.
158. Wise K.D., Sodagar A.M., Ying Y., Gulari M.N., Perlin G.E., Najafi K. Microelectrodes, microelectronics, and implantable neural microsystems. Proc. IEEE 2008, 96:1184-1202.
159. Witten I.B., Steinberg E.E., Lee S.Y., Davidson T.J., Zalocusky K.A., Brodsky M., Yizhar O., Cho S.L., Gong S., Ramakrishnan C., et al. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 2011, 72:721-733.
160. Wu F., Stark E., Im M., Cho I.J., Yoon E.S., Buzsáki G., Wise K.D., Yoon E. An implantable neural probe with monolithically integrated dielectric waveguide and recording electrodes for optogenetics applications. J.Neural Eng. 2013, 10:056012.
161. Wu F., Tien L.W., Chen F., Berke J.D., Kaplan D.L., Yoon E. Silk-backed structural optimization of high-density flexible intracortical neural probes. IEEE J. Microelectromech. Sys. 2015, 24:62-69.
162. Yamamoto J., Wilson M.A. Large-scale chronically implantable precision motorized microdrive array for freely behaving animals. J.Neurophysiol. 2008, 100:2430-2440.
163. Yao, Y., Gulari, M.N., Casey, B., Wiler, J.A., and Wise, K.D. (2007). Silicon Microelectrodes with Flexible Integrated Cables for Neural Implant Applications. In Neural Engineering, 2007 CNE '07 3rd International IEEE/EMBS Conference on, pp. 398-401.
164. Yartsev M.M., Ulanovsky N. Representation of three-dimensional space in the hippocampus of flying bats. Science 2013, 340:367-372.
165. Yuste R., Katz L.C. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 1991, 6:333-344.
166. Zemelman B.V., Lee G.A., Ng M., Miesenböck G. Selective photostimulation of genetically chARGed neurons. Neuron 2002, 33:15-22.
167. Zhang J., Laiwalla F., Kim J.A., Urabe H., Van Wagenen R., Song Y.K., Connors B.W., Zhang F., Deisseroth K., Nurmikko A.V. Integrated device for optical stimulation and spatiotemporal electrical recording of neural activity in light-sensitized brain tissue. J.Neural Eng. 2009, 6:055007.
168. Zhang F., Vierock J., Yizhar O., Fenno L.E., Tsunoda S., Kianianmomeni A., Prigge M., Berndt A., Cushman J., Polle J., et al. The microbial opsin family of optogenetic tools. Cell 2011, 147:1446-1457.
169. Zhou K., Doyle J.C., Glover K. Robust and Optimal Control 1996, Prentice Hall, Upper Saddle River, N.J.
170. Zorzos A.N., Boyden E.S., Fonstad C.G. Multiwaveguide implantable probe for light delivery to sets of distributed brain targets. Opt. Lett. 2010, 35:4133-4135.
171. Zorzos A.N., Scholvin J., Boyden E.S., Fonstad C.G. Three-dimensional multiwaveguide probe array for light delivery to distributed brain circuits. Opt. Lett. 2012, 37:4841-4843.