Abstract

Despite a potential of infrared neural stimulation (INS) for modulating neural activities, INS suffers from limited light confinement and bulk tissue heating. Here, a novel methodology for an advanced optical stimulation is proposed by combining near-infrared (NIR) stimulation with gold nanorods (GNRs) targeted to neuronal cell membrane. We confirmed experimentally that in vitro and in vivo neural activation is associated with a local heat generation based on NIR stimulation and GNRs. Compared with the case of NIR stimulation without an aid of GNRs, combination with cell-targeted GNRs allows photothermal stimulation with faster neural response, lower delivered energy, higher stimulation efficiency and stronger behavior change. Since the suggested method can reduce a requisite radiant exposure level and alleviate a concern of tissue damage, it is expected to open up new possibilities for applications to optical neuromodulations for diverse excitable tissues and treatments of neurological disorders.

© 2016 Optical Society of America

Full Article  |  PDF Article
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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  38. M. Brecht, M. Schneider, B. Sakmann, and T. W. Margrie, “Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex,” Nature 427(6976), 704–710 (2004).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2015 (1)

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
[Crossref] [PubMed]

2014 (5)

D. Jaque, L. Martínez Maestro, B. del Rosal, P. Haro-Gonzalez, A. Benayas, J. L. Plaza, E. Martín Rodríguez, and J. García Solé, “Nanoparticles for photothermal therapies,” Nanoscale 6(16), 9494–9530 (2014).
[Crossref] [PubMed]

M. M. Chernov, G. Chen, and A. W. Roe, “Histological assessment of thermal damage in the brain following infrared neural stimulation,” Brain Stimulat. 7(3), 476–482 (2014).
[Crossref] [PubMed]

K. Eom, J. Kim, J. M. Choi, T. Kang, J. W. Chang, K. M. Byun, S. B. Jun, and S. J. Kim, “Enhanced infrared neural stimulation using localized surface plasmon resonance of gold nanorods,” Small 10(19), 3853–3857 (2014).
[Crossref] [PubMed]

J. Yong, K. Needham, W. G. A. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-nanorod-assisted near-infrared stimulation of primary auditory neurons,” Adv. Healthc. Mater. 3(11), 1862–1868 (2014).
[Crossref] [PubMed]

S. Yoo, S. Hong, Y. Choi, J.-H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref] [PubMed]

2013 (6)

L. Xie, H. Kang, Q. Xu, M. J. Chen, Y. Liao, M. Thiyagarajan, J. O’Donnell, D. J. Christensen, C. Nicholson, J. J. Iliff, T. Takano, R. Deane, and M. Nedergaard, “Sleep drives metabolite clearance from the adult brain,” Science 342(6156), 373–377 (2013).
[Crossref] [PubMed]

J. J. Iliff, H. Lee, M. Yu, T. Feng, J. Logan, M. Nedergaard, and H. Benveniste, “Brain-wide pathway for waste clearance captured by contrast-enhanced MRI,” J. Clin. Invest. 123(3), 1299–1309 (2013).
[Crossref] [PubMed]

A. Blau, “Cell adhesion promotion strategies for signal transduction enhancement in microelectrode array in vitro electrophysiology: An introductory overview and critical discussion,” Curr. Opin. Colloid Interface Sci. 18(5), 481–492 (2013).
[Crossref]

X. D. Wang, O. S. Wolfbeis, and R. J. Meier, “Luminescent probes and sensors for temperature,” Chem. Soc. Rev. 42(19), 7834–7869 (2013).
[Crossref] [PubMed]

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref] [PubMed]

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3, 2600 (2013).
[PubMed]

2012 (4)

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(736), 736 (2012).
[Crossref] [PubMed]

G. Bonmassar, S. W. Lee, D. K. Freeman, M. Polasek, S. I. Fried, and J. T. Gale, “Microscopic magnetic stimulation of neural tissue,” Nat. Commun. 3, 921 (2012).
[Crossref] [PubMed]

S. A. Stanley, J. E. Gagner, S. Damanpour, M. Yoshida, J. S. Dordick, and J. M. Friedman, “Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice,” Science 336(6081), 604–608 (2012).
[Crossref] [PubMed]

J. J. Iliff, M. Wang, Y. Liao, B. A. Plogg, W. Peng, G. A. Gundersen, H. Benveniste, G. E. Vates, R. Deane, S. A. Goldman, E. A. Nagelhus, and M. Nedergaard, “A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β,” Sci. Transl. Med. 4(147), 147ra111 (2012).
[Crossref] [PubMed]

2011 (1)

C.-P. Richter, A. I. Matic, J. D. Wells, E. D. Jansen, and J. T. Walsh., “Neural stimulation with optical radiation,” Laser Photonics Rev. 5(1), 68–80 (2011).
[Crossref] [PubMed]

2010 (3)

H. Huang, S. Delikanli, H. Zeng, D. M. Ferkey, and A. Pralle, “Remote control of ion channels and neurons through magnetic-field heating of nanoparticles,” Nat. Nanotechnol. 5(8), 602–606 (2010).
[Crossref] [PubMed]

Y. Tufail, A. Matyushov, N. Baldwin, M. L. Tauchmann, J. Georges, A. Yoshihiro, S. I. H. Tillery, and W. J. Tyler, “Transcranial pulsed ultrasound stimulates intact brain circuits,” Neuron 66(5), 681–694 (2010).
[Crossref] [PubMed]

E. J. Katz, I. K. Ilev, V. Krauthamer, H. Kim, and D. Weinreich, “Excitation of primary afferent neurons by near-infrared light in vitro,” Neuroreport 21(9), 662–666 (2010).
[Crossref] [PubMed]

2009 (2)

S. E. Lee, G. L. Liu, F. Kim, and L. P. Lee, “Remote optical switch for localized and selective control of gene interference,” Nano Lett. 9(2), 562–570 (2009).
[Crossref] [PubMed]

W. M. Grill, S. E. Norman, and R. V. Bellamkonda, “Implanted neural interfaces: biochallenges and engineered solutions,” Annu. Rev. Biomed. Eng. 11(1), 1–24 (2009).
[Crossref] [PubMed]

2008 (2)

M. E. Stewart, C. R. Anderton, L. B. Thompson, J. Maria, S. K. Gray, J. A. Rogers, and R. G. Nuzzo, “Nanostructured plasmonic sensors,” Chem. Rev. 108(2), 494–521 (2008).
[Crossref] [PubMed]

S. Tandon, N. Kambi, and N. Jain, “Overlapping representations of the neck and whiskers in the rat motor cortex revealed by mapping at different anaesthetic depths,” Eur. J. Neurosci. 27(1), 228–237 (2008).
[Crossref] [PubMed]

2007 (4)

X. Han and E. S. Boyden, “Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution,” PLoS One 2(3), e299 (2007).
[Crossref] [PubMed]

J. Wells, P. Konrad, C. Kao, E. D. Jansen, and A. Mahadevan-Jansen, “Pulsed laser versus electrical energy for peripheral nerve stimulation,” J. Neurosci. Methods 163(2), 326–337 (2007).
[Crossref] [PubMed]

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39(6), 513–526 (2007).
[Crossref] [PubMed]

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref] [PubMed]

2006 (1)

A. D. Izzo, C.-P. Richter, E. D. Jansen, and J. T. Walsh., “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38(8), 745–753 (2006).
[Crossref] [PubMed]

2005 (2)

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

J. Wells, C. Kao, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Application of infrared light for in vivo neural stimulation,” J. Biomed. Opt. 10(6), 064003 (2005).
[Crossref] [PubMed]

2004 (3)

M. Brecht, M. Schneider, B. Sakmann, and T. W. Margrie, “Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex,” Nature 427(6976), 704–710 (2004).
[Crossref] [PubMed]

E. Hutter and J. H. Fendler, “Exploitation of localized surface plasmon resonance,” Adv. Mater. 16(19), 1685–1706 (2004).
[Crossref]

D. A. Wagenaar, J. Pine, and S. M. Potter, “Effective parameters for stimulation of dissociated cultures using multi-electrode arrays,” J. Neurosci. Methods 138(1-2), 27–37 (2004).
[Crossref] [PubMed]

1999 (1)

N. Kato, T. Tanaka, K. Yamamoto, and Y. Isomura, “Distinct temporal profiles of activity-dependent calcium increase in pyramidal neurons of the rat visual cortex,” J. Physiol. 519(2), 467–479 (1999).
[Crossref] [PubMed]

1998 (2)

W. S. Lee, M. K. Jain, B. M. Arkonac, D. Zhang, S.-Y. Shaw, S. Kashiki, K. Maemura, S.-L. Lee, N. K. Hollenberg, M.-E. Lee, and E. Haber, “Thy-1, a novel marker for angiogenesis upregulated by inflammatory cytokines,” Circ. Res. 82(8), 845–851 (1998).
[Crossref] [PubMed]

A. J. Verkhratsky and O. H. Petersen, “Neuronal calcium stores,” Cell Calcium 24(5-6), 333–343 (1998).
[Crossref] [PubMed]

1996 (1)

H. Kamioka, E. Maeda, Y. Jimbo, H. P. C. Robinson, and A. Kawana, “Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures,” Neurosci. Lett. 206(2-3), 109–112 (1996).
[Crossref] [PubMed]

1993 (1)

G. J. Brewer, J. R. Torricelli, E. K. Evege, and P. J. Price, “Optimized survival of hippocampal neurons in B27-supplemented neurobasalTM, a new serum-free medium combination,” J. Neurosci. Res. 35(5), 567–576 (1993).
[Crossref] [PubMed]

1991 (1)

C. G. Dotti, R. G. Parton, and K. Simons, “Polarized sorting of glypiated proteins in hippocampal neurons,” Nature 349(6305), 158–161 (1991).
[Crossref] [PubMed]

1982 (1)

K. L. Fields, D. N. Currie, and G. R. Dutton, “Development of Thy-1 antigen on cerebellar neurons in culture,” J. Neurosci. 2(6), 663–673 (1982).
[PubMed]

Anderton, C. R.

M. E. Stewart, C. R. Anderton, L. B. Thompson, J. Maria, S. K. Gray, J. A. Rogers, and R. G. Nuzzo, “Nanostructured plasmonic sensors,” Chem. Rev. 108(2), 494–521 (2008).
[Crossref] [PubMed]

Arkonac, B. M.

W. S. Lee, M. K. Jain, B. M. Arkonac, D. Zhang, S.-Y. Shaw, S. Kashiki, K. Maemura, S.-L. Lee, N. K. Hollenberg, M.-E. Lee, and E. Haber, “Thy-1, a novel marker for angiogenesis upregulated by inflammatory cytokines,” Circ. Res. 82(8), 845–851 (1998).
[Crossref] [PubMed]

Baldwin, N.

Y. Tufail, A. Matyushov, N. Baldwin, M. L. Tauchmann, J. Georges, A. Yoshihiro, S. I. H. Tillery, and W. J. Tyler, “Transcranial pulsed ultrasound stimulates intact brain circuits,” Neuron 66(5), 681–694 (2010).
[Crossref] [PubMed]

Bamberg, E.

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

Bellamkonda, R. V.

W. M. Grill, S. E. Norman, and R. V. Bellamkonda, “Implanted neural interfaces: biochallenges and engineered solutions,” Annu. Rev. Biomed. Eng. 11(1), 1–24 (2009).
[Crossref] [PubMed]

Benayas, A.

D. Jaque, L. Martínez Maestro, B. del Rosal, P. Haro-Gonzalez, A. Benayas, J. L. Plaza, E. Martín Rodríguez, and J. García Solé, “Nanoparticles for photothermal therapies,” Nanoscale 6(16), 9494–9530 (2014).
[Crossref] [PubMed]

Benveniste, H.

J. J. Iliff, H. Lee, M. Yu, T. Feng, J. Logan, M. Nedergaard, and H. Benveniste, “Brain-wide pathway for waste clearance captured by contrast-enhanced MRI,” J. Clin. Invest. 123(3), 1299–1309 (2013).
[Crossref] [PubMed]

J. J. Iliff, M. Wang, Y. Liao, B. A. Plogg, W. Peng, G. A. Gundersen, H. Benveniste, G. E. Vates, R. Deane, S. A. Goldman, E. A. Nagelhus, and M. Nedergaard, “A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β,” Sci. Transl. Med. 4(147), 147ra111 (2012).
[Crossref] [PubMed]

Bezanilla, F.

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
[Crossref] [PubMed]

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(736), 736 (2012).
[Crossref] [PubMed]

Blau, A.

A. Blau, “Cell adhesion promotion strategies for signal transduction enhancement in microelectrode array in vitro electrophysiology: An introductory overview and critical discussion,” Curr. Opin. Colloid Interface Sci. 18(5), 481–492 (2013).
[Crossref]

Bonmassar, G.

G. Bonmassar, S. W. Lee, D. K. Freeman, M. Polasek, S. I. Fried, and J. T. Gale, “Microscopic magnetic stimulation of neural tissue,” Nat. Commun. 3, 921 (2012).
[Crossref] [PubMed]

Boyden, E. S.

X. Han and E. S. Boyden, “Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution,” PLoS One 2(3), e299 (2007).
[Crossref] [PubMed]

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C.-P. Richter, A. I. Matic, J. D. Wells, E. D. Jansen, and J. T. Walsh., “Neural stimulation with optical radiation,” Laser Photonics Rev. 5(1), 68–80 (2011).
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A. D. Izzo, C.-P. Richter, E. D. Jansen, and J. T. Walsh., “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38(8), 745–753 (2006).
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X. D. Wang, O. S. Wolfbeis, and R. J. Meier, “Luminescent probes and sensors for temperature,” Chem. Soc. Rev. 42(19), 7834–7869 (2013).
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E. J. Katz, I. K. Ilev, V. Krauthamer, H. Kim, and D. Weinreich, “Excitation of primary afferent neurons by near-infrared light in vitro,” Neuroreport 21(9), 662–666 (2010).
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Wells, J.

J. Wells, P. Konrad, C. Kao, E. D. Jansen, and A. Mahadevan-Jansen, “Pulsed laser versus electrical energy for peripheral nerve stimulation,” J. Neurosci. Methods 163(2), 326–337 (2007).
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C.-P. Richter, A. I. Matic, J. D. Wells, E. D. Jansen, and J. T. Walsh., “Neural stimulation with optical radiation,” Laser Photonics Rev. 5(1), 68–80 (2011).
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J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39(6), 513–526 (2007).
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X. D. Wang, O. S. Wolfbeis, and R. J. Meier, “Luminescent probes and sensors for temperature,” Chem. Soc. Rev. 42(19), 7834–7869 (2013).
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Y. Tufail, A. Matyushov, N. Baldwin, M. L. Tauchmann, J. Georges, A. Yoshihiro, S. I. H. Tillery, and W. J. Tyler, “Transcranial pulsed ultrasound stimulates intact brain circuits,” Neuron 66(5), 681–694 (2010).
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C.-P. Richter, A. I. Matic, J. D. Wells, E. D. Jansen, and J. T. Walsh., “Neural stimulation with optical radiation,” Laser Photonics Rev. 5(1), 68–80 (2011).
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E. J. Katz, I. K. Ilev, V. Krauthamer, H. Kim, and D. Weinreich, “Excitation of primary afferent neurons by near-infrared light in vitro,” Neuroreport 21(9), 662–666 (2010).
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A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3, 2600 (2013).
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J. J. Iliff, M. Wang, Y. Liao, B. A. Plogg, W. Peng, G. A. Gundersen, H. Benveniste, G. E. Vates, R. Deane, S. A. Goldman, E. A. Nagelhus, and M. Nedergaard, “A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β,” Sci. Transl. Med. 4(147), 147ra111 (2012).
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L. Xie, H. Kang, Q. Xu, M. J. Chen, Y. Liao, M. Thiyagarajan, J. O’Donnell, D. J. Christensen, C. Nicholson, J. J. Iliff, T. Takano, R. Deane, and M. Nedergaard, “Sleep drives metabolite clearance from the adult brain,” Science 342(6156), 373–377 (2013).
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S. A. Stanley, J. E. Gagner, S. Damanpour, M. Yoshida, J. S. Dordick, and J. M. Friedman, “Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice,” Science 336(6081), 604–608 (2012).
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Figures (7)

Fig. 1
Fig. 1 Optical stimulation of neuron using surface-modified GNRs. (a) Streptavidin coated gold nanorods (GNRs) are delivered to the neuron by biotinylated anti-Thy-1 antibody that bind to an epitope from external neuronal membrane. Localized heat from strongly bound GNRs could elicit neuronal depolarization. (b) TEM image reveals that average geometric dimensions of GNRs are 80.4 nm in length and 15.3 nm in width. Optical extinction spectrum of GNRs shows a longitudinal absorption peak at λ = 977 nm. (c) The phase contrast microscope image shows a typical hippocampal neural cell after 18 days in vitro. Cell bodies as well as axons can be distinguished morphologically. (d) After neuronal membrane is tagged by biotinylated anti-Thy1.1 antibody, streptavidin-coated GNRs are incubated to form a strong binding with biotinylated antibody. Biotinylated FITC is used to observe the distribution of streptavidin-coated GNRs. Scale bar, 100 μm in (c) and (d).
Fig. 2
Fig. 2 Experimental setup of stimulation and recording for cultured hippocampal neuron. Neuron is cultured on MEAs and pulsed NIR light is irradiated by fiber-coupled laser diode. Stimulus-triggered neural activities are recorded from the MEA. For electrical stimulation and recording, stimulus is delivered through the one of electrodes and stimulus triggered neural responses are recorded from the rest of the electrodes in MEA.
Fig. 3
Fig. 3 Experimental setup of optical stimulation and recording system for rat vibrissae motor cortex in vivo. GNRs are injected (anteriorly 2.9 mm, laterally 1.5 mm, and 1.0 mm in depth relative to bregma, indicated by a yellow ellipse) prior to the optical stimulation. Whisker trajectories monitored by CCD camera, angle change between the resting and activating states (indicated by two dotted lines) are extracted.
Fig. 4
Fig. 4 Characteristic of neural response upon electrical stimulus. (a) An inter-burst interval histogram without electrical stimulation reveals that burst fires every 10.8 s. (b) Evoked action potentials after electrical stimulation (Stimulus parameters: anodic-first biphasic current stimulation pulse, current amplitude of 20 μA, and a width of 200 μs per phase) show neurons fire immediately after stimulus. (c) A post-stimulus time histogram to show the temporal distribution of electrically evoked action potentials. Neurons respond to the electrical stimuli having latency (time to get the maximum spikes after stimulus) of 25 ms.
Fig. 5
Fig. 5 Characteristic of neural response upon optical stimulus with and without cell-targeted GNRs. (a) Evoked action potentials after optical stimulation without cell-targeted GNRs show neurons are sensitive to optical stimulus and trigger neural activities at the threshold intensity of 46.9 mJ/cm2. (b) A post-stimulus time histogram to show the temporal distribution of optically evoked action potentials. Neurons respond to the optical stimuli having latency (time to get the maximum spikes after stimulus) of 265 ms. (c) Evoked action potentials after optical stimulation with cell-targeted GNRs show neurons fire right after stimulation with small temporal jitter. Laser threshold intensity used to evoke neural response is 30.1 mJ/cm2 which is about the half of the laser intensity stimulating without cell-targeted GNRs. (d) A post-stimulus time histogram to shows reduced latency of 95 ms.
Fig. 6
Fig. 6 Whisker movement evoked by optical and electrical stimulation of rat vibrissae motor cortex in vivo. (a) Whisker trajectories according to optical stimulation with and without antibody-conjugated GNRs. Optical stimuli (indicated by yellow line) are applied with train of fifteen pulses at 300 Hz with pulse duration of 1.5 ms and a period between the trains of 2 s. (b) Whisker trajectories when electrical stimuli are applied with 66.7 ms train of twenty monophasic, negative, 0.2 ms pulses at 300 Hz with amplitude of 2.4 mA.
Fig. 7
Fig. 7 Characterization of local heat generation by GNRs. (a) Temperature dependence of fluorescent intensity of biotinylated FITC shows a linear decrement of normalized fluorescent intensity upon temperature increment. (b) Temperature profiles are measured from temperature-sensitive fluorescent dyes before and after illuminating laser (indicated by yellow line) in solutions with and without GNRs. Temperature is monitored by capturing average fluorescent intensity with a frequency of 500 Hz.

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