1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biomedical Engineering
  4. Volume 16, 2014
  5. Article

Annual Review of Biomedical Engineering

Volume 16, 2014

Optical Neural Interfaces

Abstract

Genetically encoded optical actuators and indicators have changed the landscape of neuroscience, enabling targetable control and readout of specific components of intact neural circuits in behaving animals. Here, we review the development of optical neural interfaces, focusing on hardware designed for optical control of neural activity, integrated optical control and electrical readout, and optical readout of population and single-cell neural activity in freely moving mammals.

Keyword(s): channelrhodopsin, GCaMP, halorhodopsin, imaging, neurophysiology, optogenetics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-071813-104733
2014-07-11
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/16/1/annurev-bioeng-071813-104733.html?itemId=/content/journals/10.1146/annurev-bioeng-071813-104733&mimeType=html&fmt=ahah

Literature Cited

  1. Penfield W, Perot P. 1.  1963. The brain's record of auditory and visual experience: a final summary and discussion. Brain 86:4595–696 [Google Scholar]
  2. Salzman CD, Britten KH, Newsome WT. 2.  1990. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346:6280174–77 [Google Scholar]
  3. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D. 3.  et al. 2005. Deep brain stimulation for treatment-resistant depression. Neuron 45:5651–60 [Google Scholar]
  4. Fenno L, Yizhar O, Deisseroth K. 4.  2011. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389–412 [Google Scholar]
  5. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. 5.  2011. Optogenetics in neural systems. Neuron 71:19–34 [Google Scholar]
  6. Knöpfel T. 6.  2012. Genetically encoded optical indicators for the analysis of neuronal circuits. Nat. Rev. Neurosci. 13:10687–700 [Google Scholar]
  7. Looger LL, Griesbeck O. 7.  2012. Genetically encoded neural activity indicators. Curr. Opin. Neurobiol. 22:118–23 [Google Scholar]
  8. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 8.  2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:91263–68 [Google Scholar]
  9. Zhang F, Wang L-P, Brauner M, Liewald JF, Kay K. 9.  et al. 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446:7136633–39 [Google Scholar]
  10. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM. 10.  et al. 2002. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:55772395–98 [Google Scholar]
  11. Han X, Boyden ES. 11.  2007. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2:3e299 [Google Scholar]
  12. Zhang F, Prigge M, Beyrière F, Tsunoda SP, Mattis J. 12.  et al. 2008. Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat. Neurosci. 11:6631–33 [Google Scholar]
  13. Berndt A, Yizhar O, Gunaydin L, Hegemann P, Deisseroth K. 13.  2009. Bi-stable neural state switches. Nat. Neurosci. 12:2229–34 [Google Scholar]
  14. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R. 14.  et al. 2010. Molecular and cellular principles for diversifying and extending optogenetics. Cell 141:1–12 [Google Scholar]
  15. Chow BY, Han X, Dobry AS, Qian X, Chuong AS. 15.  et al. 2010. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463:727798–102 [Google Scholar]
  16. Lin JY, Lin MZ, Steinbach P, Tsien RY. 16.  2009. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96:51803–14 [Google Scholar]
  17. Wang H, Sugiyama Y, Hikima T, Sugano E, Tomita H. 17.  et al. 2009. Molecular determinants differentiating photocurrent properties of two channelrhodopsins from Chlamydomonas. J. Biol. Chem. 284:95685–96 [Google Scholar]
  18. Gunaydin L, Yizhar O, Berndt A, Sohal VS, Deisseroth K, Hegemann P. 18.  2010. Ultrafast optogenetic control. Nat. Neurosci. 13:3387–92 [Google Scholar]
  19. Berndt A, Schoenenberger P, Mattis J, Tye KM, Deisseroth K. 19.  et al. 2011. High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 108:187595–600 [Google Scholar]
  20. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ. 20.  et al. 2011. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:7363171–78 [Google Scholar]
  21. Mattis J, Tye KM, Ferenczi E, Ramakrishnan C, O'Shea DJ. 21.  et al. 2012. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 9:2159–72 [Google Scholar]
  22. Zemelman BV, Lee GA, Ng M, Miesenböck G. 22.  2002. Selective photostimulation of genetically charged neurons. Neuron 33:115–22 [Google Scholar]
  23. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH. 23.  2004. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7:121381–86 [Google Scholar]
  24. Lima SQ, Miesenböck G. 24.  2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:1141–52 [Google Scholar]
  25. Prigge M, Schneider F, Tsunoda SP, Shilyansky C, Wietek J. 25.  et al. 2012. Color-tuned channelrhodopsins for multiwavelength optogenetics. J. Biol. Chem. 287:3831804–12 [Google Scholar]
  26. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 26.  2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15:242279–84 [Google Scholar]
  27. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. 27.  2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450:7168420–24 [Google Scholar]
  28. Aravanis AM, Wang LP, Zhang F, Meltzer LA, Mogri MZ. 27a.  et al. 2007. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J. Neural Eng. 4:S143–56 [Google Scholar]
  29. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K. 28.  et al. 2007. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27:5214231–38 [Google Scholar]
  30. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD. 29.  et al. 2010. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 5:3439–56 [Google Scholar]
  31. Sparta DR, Stamatakis AM, Phillips JL, Hovelsø N, Van Zessen R, Stuber GD. 30.  2012. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 7:112–23 [Google Scholar]
  32. Witten IB, Lin S-C, Brodsky M, Prakash R, Diester I. 31.  et al. 2010. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330:60111677–81 [Google Scholar]
  33. Tye KM, Prakash R, Kim S-Y, Fenno LE, Grosenick L. 32.  et al. 2011. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:7338358–62 [Google Scholar]
  34. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V. 33.  et al. 2011. Dynamics of retrieval strategies for remote memories. Cell 147:3678–89 [Google Scholar]
  35. Warden MR, Selimbeyoglu A, Mirzabekov JJ, Lo M, Thompson KR. 34.  et al. 2012. A prefrontal cortex–brainstem neuronal projection that controls response to behavioural challenge. Nature 492:7429428–32 [Google Scholar]
  36. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai H-C. 35.  et al. 2013. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493:7433537–41 [Google Scholar]
  37. Kim S-Y, Adhikari A, Lee SY, Marshel JH, Kim CK. 36.  et al. 2013. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496:7444219–23 [Google Scholar]
  38. Wentz CT, Bernstein JG, Monahan P, Guerra A, Rodriguez A, Boyden ES. 37.  2011. A wirelessly powered and controlled device for optical neural control of freely-behaving animals. J. Neural Eng. 8:4046021 [Google Scholar]
  39. Clements I, Gnade A, Rush A, Patten C, Twomey M, Kravitz A. 38.  2013. Miniaturized LED sources for in vivo optogenetic experimentation. Proc. SPIE 8586:85860 [Google Scholar]
  40. Huber D, Petreanu L, Ghitani N, Ranade S, Hromádka T. 39.  et al. 2008. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451:717461–64 [Google Scholar]
  41. Bernstein JG, Han X, Henninger M, Ko EY, Qian X. 40.  et al. 2008. Prosthetic systems for therapeutic optical activation and silencing of genetically-targeted neurons. Proc. Soc. Photo-Opt. Instrum. Eng. 6854:68540H [Google Scholar]
  42. Iwai Y, Honda S, Ozeki H, Hashimoto M, Hirase H. 41.  2011. A simple head-mountable LED device for chronic stimulation of optogenetic molecules in freely moving mice. Neurosci. Res. 70:1124–27 [Google Scholar]
  43. Bernstein JG, Boyden ES. 42.  2011. Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn. Sci. 15:12592–600 [Google Scholar]
  44. Zorzos AN, Boyden ES, Fonstad CG. 43.  2010. Multiwaveguide implantable probe for light delivery to sets of distributed brain targets. Opt. Lett. 35:244133–35 [Google Scholar]
  45. Zorzos AN, Scholvin J, Boyden ES, Fonstad CG. 44.  2012. Three-dimensional multiwaveguide probe array for light delivery to distributed brain circuits. Opt. Lett. 37:234841–43 [Google Scholar]
  46. Im M, Cho I, Wu F, Wise KD, Yoon E. 45.  2011. Neural probes integrated with optical mixer/splitter waveguides and multiple stimulation sites. Proc. Int. Conf. Micro Electro Mech. Syst. (MEMS), 24th, Cancun, Mex., Jan. 23–271051–54 New York: IEEE [Google Scholar]
  47. Abaya TVF, Blair S, Tathireddy P, Rieth L, Solzbacher F. 46.  2012. A 3D glass optrode array for optical neural stimulation. Biomed. Opt. Express 3:123087–104 [Google Scholar]
  48. Abaya TVF, Diwekar M, Blair S, Tathireddy P, Rieth L. 47.  et al. 2012. Characterization of a 3D optrode array for infrared neural stimulation. Biomed. Opt. Express 3:92200–19 [Google Scholar]
  49. Kim T-I, McCall JG, Jung YH, Huang X, Siuda ER. 48.  et al. 2013. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 340:6129211–16 [Google Scholar]
  50. Ungless MA, Grace AA. 49.  2012. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci. 35:7422–30 [Google Scholar]
  51. Grace AA, Bunney BS. 50.  1980. Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence. Science 210:4470654–56 [Google Scholar]
  52. Swadlow HA. 51.  1998. Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification. J. Neurosci. Methods 79:2131–41 [Google Scholar]
  53. Diester I, Nieder A. 52.  2008. Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J. Neurosci. 28:317737–47 [Google Scholar]
  54. Constantinidis C, Goldman-Rakic PS. 53.  2002. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J. Neurophysiol. 88:63487–97 [Google Scholar]
  55. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 54.  2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:738385–88 [Google Scholar]
  56. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. 55.  2009. Optical deconstruction of parkinsonian neural circuitry. Science 324:5925354–59 [Google Scholar]
  57. Tsai H-C, Zhang F, Adamantidis A, Stuber GD, Bonci A. 56.  et al. 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:59301080–84 [Google Scholar]
  58. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F. 57.  et al. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:7247663–67 [Google Scholar]
  59. Royer S, Zemelman BV, Barbic M, Losonczy A, Buzsáki G, Magee JC. 58.  2010. Multi-array silicon probes with integrated optical fibers: light-assisted perturbation and recording of local neural circuits in the behaving animal. Eur. J. Neurosci. 31:122279–91 [Google Scholar]
  60. Halassa MM, Siegle JH, Ritt JT, Ting JT, Feng G, Moore CI. 59.  2011. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat. Neurosci. 14:91118–20 [Google Scholar]
  61. Siegle JH, Carlen M, Meletis K, Tsai L-H, Moore CI, Ritt J. 60.  2011. Chronically implanted hyperdrive for cortical recording and optogenetic control in behaving mice. Proc. Annu. Int. Conf. Eng. Med. Biol. Soc. (EMBS), 33rd, Boston, Aug. 30–Sep. 37529–32 New York: IEEE [Google Scholar]
  62. Anikeeva P, Andalman AS, Witten I, Warden M, Goshen I. 61.  et al. 2012. Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15:1163–70 [Google Scholar]
  63. Stark E, Koos T, Buzsáki G. 62.  2012. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J. Neurophysiol. 108:1349–63 [Google Scholar]
  64. Voigts J, Siegle JH, Pritchett DL, Moore CI. 63.  2013. The flexDrive: an ultra-light implant for optical control and highly parallel chronic recording of neuronal ensembles in freely moving mice. Front. Syst. Neurosci. 7:8 [Google Scholar]
  65. Wang J, Borton DA, Zhang J, Burwell RD, Nurmikko AV. 64.  2010. A neurophotonic device for stimulation and recording of neural microcircuits. Proc. Annu. Int. Conf. Eng. Med. Biol. Soc. (EMBS), 32nd, Buenos Aires, Aug. 31–Sep. 42935–38 New York: IEEE [Google Scholar]
  66. Wang J, Wagner F, Borton D, Zhang J, Ozden I. 65.  et al. 2012. Integrated device for combined optical neuromodulation and electrical recording for chronic in vivo applications. J. Neural Eng. 9:1016001 [Google Scholar]
  67. Csicsvari J, Henze DA, Jamieson B, Harris KD, Sirota A. 66.  et al. 2003. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 90:21314–23 [Google Scholar]
  68. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G. 67.  2004. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J. Neurophysiol. 92:1600–8 [Google Scholar]
  69. McNaughton BL, O'Keefe J, Barnes C. 68.  1983. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Methods 8:4391–97 [Google Scholar]
  70. Wilson M, McNaughton BL. 69.  1993. Dynamics of the hippocampal ensemble code for space. Science 261:51241055–58 [Google Scholar]
  71. Kloosterman F, Davidson TJ, Gomperts SN, Layton SP, Hale G. 70.  et al. 2009. Micro-drive array for chronic in vivo recording: drive fabrication. J. Vis. Exp.26e1094
  72. Nguyen DP, Layton SP, Hale G, Gomperts SN, Davidson TJ. 71.  et al. 2009. Micro-drive array for chronic in vivo recording: tetrode assembly. J. Vis. Exp.26e1098
  73. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F. 72.  et al. 2010. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of channelrhodopsin-2. Nat. Protoc. 5:2247–54 [Google Scholar]
  74. Han X, Qian X, Bernstein JG, Zhou H-H, Franzesi GT. 73.  et al. 2009. Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain. Neuron 62:2191–98 [Google Scholar]
  75. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA. 74.  et al. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:6645882–87 [Google Scholar]
  76. Persechini A, Lynch JA, Romoser VA. 75.  1997. Novel fluorescent indicator proteins for monitoring free intracellular Ca2+. Cell Calcium 22:3209–16 [Google Scholar]
  77. Romoser VA. 76.  1997. Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence: a new class of fluorescent indicators. J. Biol. Chem. 272:2013270–74 [Google Scholar]
  78. Nakai J, Ohkura M, Imoto K. 77.  2001. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19:2137–41 [Google Scholar]
  79. Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J. 78.  2005. Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal. Chem. 77:185861–69 [Google Scholar]
  80. Tallini YN, Ohkura M, Choi B-R, Ji G, Imoto K. 79.  et al. 2006. Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc. Natl. Acad. Sci. USA 103:124753–58 [Google Scholar]
  81. Zhao Y, Araki S, Wu J, Teramoto T, Chang Y-F. 80.  et al. 2011. An expanded palette of genetically encoded Ca2+ indicators. Science 333:60511888–91 [Google Scholar]
  82. Akerboom J, Chen T-W, Wardill TJ, Tian L, Marvin JS. 81.  et al. 2012. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32:4013819–40 [Google Scholar]
  83. Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M. 82.  et al. 2013. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6:2 [Google Scholar]
  84. Hires SA, Tian L, Looger LL. 83.  2008. Reporting neural activity with genetically encoded calcium indicators. Brain Cell Biol. 36:1–469–86 [Google Scholar]
  85. Tian L, Hires SA, Mao T, Huber D, Chiappe ME. 84.  et al. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6:12875–81 [Google Scholar]
  86. Tian L, Akerboom J, Schreiter ER, Looger LL. 85.  2012. Neural activity imaging with genetically encoded calcium indicators. Prog. Brain Res. 196:79–94 [Google Scholar]
  87. Tian L, Hires SA, Looger LL. 86.  2012. Imaging neuronal activity with genetically encoded calcium indicators. Cold Spring Harb. Protoc. 2012:6647–56 [Google Scholar]
  88. Dugué GP, Akemann W, Knöpfel T. 87.  2012. A comprehensive concept of optogenetics. Prog. Brain Res. 196:1–28 [Google Scholar]
  89. Alford SC, Wu J, Zhao Y, Campbell RE, Knöpfel T. 88.  2013. Optogenetic reporters. Biol. Cell 105:114–29 [Google Scholar]
  90. Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL. 89.  et al. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:7458295–300 [Google Scholar]
  91. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT. 90.  et al. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10:2162–70 [Google Scholar]
  92. Adelsberger H, Garaschuk O, Konnerth A. 91.  2005. Cortical calcium waves in resting newborn mice. Nat. Neurosci. 8:8988–90 [Google Scholar]
  93. Ferezou I, Bolea S, Petersen CCH. 92.  2006. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50:4617–29 [Google Scholar]
  94. Murayama M, Pérez-Garci E, Lüscher H-R, Larkum ME. 93.  2007. Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. J. Neurophysiol. 98:31791–805 [Google Scholar]
  95. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, Larkum ME. 93a.  2009. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457:1137–41 [Google Scholar]
  96. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE. 94.  et al. 2014. Natural neural projection dynamics underlying social behavior Cell.In press [Google Scholar]
  97. Lütcke H, Murayama M, Hahn T, Margolis DJ, Astori S. 95.  et al. 2010. Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Front. Neural Circuits 4:9 [Google Scholar]
  98. Cui G, Jun SB, Jin X, Pham MD, Vogel SS. 96.  et al. 2013. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494:7436238–42 [Google Scholar]
  99. Helmchen F, Fee MS, Tank DW, Denk W. 97.  2001. A miniature head-mounted two-photon microscope: high-resolution brain imaging in freely moving animals. Neuron 31:6903–12 [Google Scholar]
  100. Flusberg BA, Jung JC, Cocker ED, Anderson EP, Schnitzer MJ. 98.  2005. In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. Opt. Lett. 30:172272–74 [Google Scholar]
  101. Flusberg BA, Nimmerjahn A, Cocker ED, Mukamel EA, Barretto RPJ. 99.  et al. 2008. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods 5:11935–38 [Google Scholar]
  102. Sawinski J, Wallace DJ, Greenberg DS, Grossmann S, Denk W, Kerr JND. 100.  2009. Visually evoked activity in cortical cells imaged in freely moving animals. Proc. Natl. Acad. Sci. USA 106:4619557–62 [Google Scholar]
  103. Ghosh KK, Burns LD, Cocker ED, Nimmerjahn A, Ziv Y. 101.  et al. 2011. Miniaturized integration of a fluorescence microscope. Nat. Methods 8:10871–78 [Google Scholar]
  104. Jung JC, Mehta AD, Aksay E, Stepnoski R, Schnitzer MJ. 102.  2004. In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. J. Neurophysiol. 92:53121–33 [Google Scholar]
  105. Kerr JND, Nimmerjahn A. 103.  2012. Functional imaging in freely moving animals. Curr. Opin. Neurobiol. 22:145–53 [Google Scholar]
  106. Lütcke H, Margolis DJ, Helmchen F. 104.  2013. Steady or changing? Long-term monitoring of neuronal population activity. Trends Neurosci. 36:7375–84 [Google Scholar]
  107. Regehr WG, Tank DW. 105.  1991. Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J. Neurosci. Methods 37:111–19 [Google Scholar]
  108. O'Donovan MJ, Ho S, Sholomenko G, Yee W. 106.  1993. Real-time imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes. J. Neurosci. Methods 46:291–106 [Google Scholar]
  109. Nimmerjahn A, Kirchhoff F, Kerr JND, Helmchen F. 107.  2004. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1:131–37 [Google Scholar]
  110. Wallace DJ, Meyer zum Alten Borgloh S, Astori S, Yang Y, Bausen M. 108.  et al. 2008. Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor. Nat. Methods 5:9797–804 [Google Scholar]
  111. Hasan MT, Friedrich RW, Euler T, Larkum ME, Giese G. 109.  et al. 2004. Functional fluorescent Ca2+ indicator proteins in transgenic mice under TET control. PLoS Biol. 2:6e163 [Google Scholar]
  112. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L. 110.  et al. 2012. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32:93131–41 [Google Scholar]
  113. Jaffe DB, Johnston D, Lasser-Ross N, Lisman JE, Miyakawa H, Ross WN. 111.  1992. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature 357:6375244–46 [Google Scholar]
  114. Denk W, Yuste R, Svoboda K, Tank DW. 112.  1996. Imaging calcium dynamics in dendritic spines. Curr. Opin. Neurobiol. 6:3372–78 [Google Scholar]
  115. Wu J, Liu L, Matsuda T, Zhao Y, Rebane A. 113.  et al. 2013. Improved orange and red Ca2+ indicators and photophysical considerations for optogenetic applications. ACS Chem. Neurosci. 4:6963–72 [Google Scholar]
  116. Ohkura M, Sasaki T, Kobayashi C, Ikegaya Y, Nakai J. 114.  2012. An improved genetically encoded red fluorescent Ca2+ indicator for detecting optically evoked action potentials. PLoS ONE 7:7e39933 [Google Scholar]
  117. Li Y, Tsien RW. 115.  2012. pHTomato, a red, genetically encoded indicator that enables multiplex interrogation of synaptic activity. Nat. Neurosci. 15:71047–53 [Google Scholar]
  118. Hires SA, Zhu Y, Tsien RY. 116.  2008. Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc. Natl. Acad. Sci. USA 105:114411–16 [Google Scholar]
  119. Ungerstedt U. 117.  1984. Measurement of neurotransmitter release by intracranial dialysis. Measurement of Neurotransmitter Release In Vivo CA Marsden 81–107 New York: Wiley [Google Scholar]
  120. Moghaddam B, Bunney BS. 118.  1990. Acute effects of typical and atypical antipsychotic drugs on the release of dopamine from prefrontal cortex, nucleus accumbens, and striatum of the rat: an in vivo microdialysis study. J. Neurochem. 54:51755–60 [Google Scholar]
  121. Stamford JA, Justice JB. 119.  1996. Probing brain chemistry. Anal. Chem. 68:11359A–63A [Google Scholar]
  122. Phillips PEM, Stuber GD, Heien MLAV, Wightman RM, Carelli RM. 120.  2003. Subsecond dopamine release promotes cocaine seeking. Nature 422:6932614–18 [Google Scholar]
  123. Siegel MS, Isacoff EY. 121.  1997. A genetically encoded optical probe of membrane voltage. Neuron 19:4735–41 [Google Scholar]
  124. Cacciatore TW, Brodfuehrer PD, Gonzalez JE, Jiang T, Adams SR. 122.  et al. 1999. Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes. Neuron 23:3449–59 [Google Scholar]
  125. Sakai R, Repunte-Canonigo V, Raj CD, Knöpfel T. 123.  2001. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur. J. Neurosci. 13:122314–18 [Google Scholar]
  126. Ataka K, Pieribone VA. 124.  2002. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys. J. 82:1509–16 [Google Scholar]
  127. Akemann W, Mutoh H, Perron A, Rossier J, Knöpfel T. 125.  2010. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 7:8643–49 [Google Scholar]
  128. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE. 126.  2011. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333:6040345–48 [Google Scholar]
  129. Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE. 127.  2012. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 9:190–95 [Google Scholar]
  130. Perron A, Akemann W, Mutoh H, Knöpfel T. 128.  2012. Genetically encoded probes for optical imaging of brain electrical activity. Prog. Brain Res. 196:63–77 [Google Scholar]
  131. Gong Y, Li JZ, Schnitzer MJ. 129.  2013. Enhanced archaerhodopsin fluorescent protein voltage indicators. PLoS ONE 8:6e66959 [Google Scholar]
  132. Baker BJ, Kosmidis EK, Vucinic D, Falk CX, Cohen LB. 130.  et al. 2005. Imaging brain activity with voltage- and calcium-sensitive dyes. Cell. Mol. Neurobiol. 25:2245–82 [Google Scholar]
  133. Froemke RC, Kumar VS, Czkwianianc P, Yuste R. 131.  2002. Analysis of multineuronal activation patterns from calcium-imaging experiments in brain slices. Trends Cardiovasc. Med. 12:6247–52 [Google Scholar]
  134. Stosiek C, Garaschuk O, Holthoff K, Konnerth A. 132.  2003. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100:7319–24 [Google Scholar]
  135. Duff Davis M, Schmidt JJ. 133.  2000. In vivo spectrometric calcium flux recordings of intrinsic caudate-putamen cells and transplanted IMR-32 neuroblastoma cells using miniature fiber optrodes in anesthetized and awake rats and monkeys. J. Neurosci. Methods 99:1–29–23 [Google Scholar]
  136. Hirano M, Yamashita Y, Miyakawa A. 134.  1996. In vivo visualization of hippocampal cells and dynamics of Ca2+ concentration during anoxia: feasibility of a fiber-optic plate microscope system for in vivo experiments. Brain Res. 732:1–261–68 [Google Scholar]
  137. Denk W, Svoboda K. 135.  1997. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18:3351–57 [Google Scholar]
  138. Svoboda K, Yasuda R. 136.  2006. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 50:6823–39 [Google Scholar]
  139. Flusberg BA, Cocker ED, Piyawattanametha W, Jung JC, Cheung ELM, Schnitzer MJ. 137.  2005. Fiber-optic fluorescence imaging. Nat. Methods 2:12941–50 [Google Scholar]
  140. Denk W, Strickler JH, Webb WW. 138.  1990. Two-photon laser scanning fluorescence microscopy. Science 248:495173–76 [Google Scholar]
  141. Svoboda K, Denk W, Kleinfeld D, Tank DW. 139.  1997. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:6612161–65 [Google Scholar]
  142. Kleinfeld D, Mitra PP, Helmchen F, Denk W. 140.  1998. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. USA 95:2615741–46 [Google Scholar]
  143. Dombeck D, Khabbaz AN, Collman F, Adelman TL, Tank DW. 141.  2007. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56:143–57 [Google Scholar]
  144. Laffray S, Pagès S, Dufour H, De Koninck P, De Koninck Y, Côté D. 142.  2011. Adaptive movement compensation for in vivo imaging of fast cellular dynamics within a moving tissue. PLoS ONE 6:5e19928 [Google Scholar]
  145. Paukert M, Bergles DE. 143.  2012. Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning. J. Physiol. 590:2955–63 [Google Scholar]
  146. Chen JL, Pfaffli OA, Voigt FF, Margolis DJ, Helmchen F. 144.  2013. Online correction of licking-induced brain motion during two-photon imaging with a tunable lens. J. Physiol. 591:194689–98 [Google Scholar]
  147. Levene MJ, Dombeck D, Kasischke KA, Molloy RP, Webb WW. 145.  2004. In vivo multiphoton microscopy of deep brain tissue. J. Neurophysiol. 91:41908–12 [Google Scholar]
  148. Ziv Y, Burns LD, Cocker ED, Hamel EO, Ghosh KK. 146.  et al. 2013. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 16:3264–66 [Google Scholar]
  149. Towne C, Montgomery KL, Iyer SM, Deisseroth K, Delp SL. 147.  2013. Optogenetic control of targeted peripheral axons in freely moving animals. PLoS ONE 8:8e72691 [Google Scholar]
  150. Liske H, Towne C, Anikeeva P, Zhao S, Feng G. 148.  et al. 2013. Optical inhibition of motor nerve and muscle activity in vivo. Muscle Nerve 47:6916–21 [Google Scholar]
  151. Llewellyn ME, Thompson KR, Deisseroth K, Delp SL. 149.  2010. Orderly recruitment of motor units under optical control in vivo. Nat Med. 16:101161–65 [Google Scholar]
  152. Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N. 150.  et al. 2012. Two-photon optogenetic toolbox for fast inhibition, excitation, and bistable modulation. Nat. Methods 9:1171–79 [Google Scholar]
  153. Packer AM, Peterka DS, Hirtz JJ, Prakash R, Deisseroth K, Yuste R. 151.  2012. Two-photon optogenetics of dendritic spines and neuronal circuits in 3D. Nat. Methods 9:121202–5 [Google Scholar]
  154. Deisseroth K, Schnitzer M. 152.  2013. Engineering approaches to illuminating brain structure and dynamics. Neuron 80:3568–77 [Google Scholar]
  155. Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K. 153.  2009. Temporally precise in vivo control of intracellular signaling. Nature 458:1025–29 [Google Scholar]
  156. Zhang F, Aravanis AM, Adamantidis A, de Lecea L, Deisseroth K. 154.  2007. Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 8:8577–81 [Google Scholar]
/content/journals/10.1146/annurev-bioeng-071813-104733
Loading
Optical Neural Interfaces
Annual Review of Biomedical Engineering 16, 103 (2014); https://doi.org/10.1146/annurev-bioeng-071813-104733
/content/journals/10.1146/annurev-bioeng-071813-104733
/content/journals/10.1146/annurev-bioeng-071813-104733
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error