Abstract

We demonstrate optical fine-needle imaging biopsy (FNIB), combining a fine needle (22 gauge) and a high-resolution side-view probe (350-μm diameter) for minimally invasive interrogation of brain tissue in situ. We apply this technique to examine pathogenesis in murine models of neurodegeneration, brain metastasis of melanoma, and arterial occlusion, respectively. The demonstrated ability to obtain cellular images in the deep brain without craniotomy may be useful in the longitudinal studies of brain diseases.

© 2013 Optical Society of America

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  1. J. Tilgner, M. Herr, C. Ostertag, and B. Volk, “Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors,” Neurosurgery56(2), 257–265, discussion 257–265 (2005).
    [CrossRef] [PubMed]
  2. W. Feiden, U. Steude, K. Bise, and O. Gündisch, “Accuracy of stereotactic brain tumor biopsy: comparison of the histologic findings in biopsy cylinders and resected tumor tissue,” Neurosurg. Rev.14(1), 51–56 (1991).
    [PubMed]
  3. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods2(12), 932–940 (2005).
    [CrossRef] [PubMed]
  4. A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
    [CrossRef] [PubMed]
  5. G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc.5(2), 201–208 (2010).
    [CrossRef] [PubMed]
  6. R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
    [CrossRef] [PubMed]
  7. L. Fu, A. Jain, C. Cranfield, H. K. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt.12(4), 040501 (2007).
    [CrossRef] [PubMed]
  8. J. K. Kim, W. M. Lee, P. Kim, M. Choi, K. Jung, S. Kim, and S. H. Yun, “Fabrication and operation of GRIN probes for in vivo fluorescence cellular imaging of internal organs in small animals,” Nat. Protoc.7(8), 1456–1469 (2012).
    [CrossRef] [PubMed]
  9. J. K. Kim J. W. Choi and S. H. Yun, “350 μm sideview optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt.18, 050502 (2013).
    [CrossRef]
  10. P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt.13(1), 010501 (2008).
    [CrossRef] [PubMed]
  11. K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
    [CrossRef] [PubMed]
  12. A. Hara, M. Niwa, N. Yoshimi, and H. Mori, “Apoptotic cell death in vulnerable subpopulation of cerebellar granule cells,” Acta Neuropathol.94(5), 517–518 (1997).
    [CrossRef] [PubMed]
  13. L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
    [PubMed]
  14. T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
    [CrossRef] [PubMed]
  15. G. Stoll, C. Kleinschnitz, and B. Nieswandt, “Combating innate inflammation: a new paradigm for acute treatment of stroke?” Ann. N. Y. Acad. Sci.1207(1), 149–154 (2010).
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  16. R. Jin, G. Yang, and G. Li, “Inflammatory mechanisms in ischemic stroke: role of inflammatory cells,” J. Leukoc. Biol.87(5), 779–789 (2010).
    [CrossRef] [PubMed]
  17. A. F. Eichler, E. Chung, D. P. Kodack, J. S. Loeffler, D. Fukumura, and R. K. Jain, “The biology of brain metastases-translation to new therapies,” Nat Rev Clin Oncol8(6), 344–356 (2011).
    [PubMed]
  18. Y. Chudnovsky, P. A. Khavari, and A. E. Adams, “Melanoma genetics and the development of rational therapeutics,” J. Clin. Invest.115(4), 813–824 (2005).
    [PubMed]
  19. T. H. Chia and M. J. Levene, “Microprisms for in vivo multilayer cortical imaging,” J. Neurophysiol.102(2), 1310–1314 (2009).
    [CrossRef] [PubMed]
  20. D. E. Bredesen, R. V. Rao, and P. Mehlen, “Cell death in the nervous system,” Nature443(7113), 796–802 (2006).
    [CrossRef] [PubMed]
  21. K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
    [CrossRef] [PubMed]
  22. M. Fuhrmann, T. Bittner, C. K. E. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms, “Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease,” Nat. Neurosci.13(4), 411–413 (2010).
    [CrossRef] [PubMed]
  23. M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
    [CrossRef] [PubMed]
  24. E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet, “Cerebrovascular disorders: molecular insights and therapeutic opportunities,” Nat. Neurosci.14(11), 1390–1397 (2011).
    [CrossRef] [PubMed]
  25. I. J. Fidler, G. Schackert, R. D. Zhang, R. Radinsky, and T. Fujimaki, “The biology of melanoma brain metastasis,” Cancer Metastasis Rev.18(3), 387–400 (1999).
    [CrossRef] [PubMed]
  26. R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods6(7), 511–512 (2009).
    [CrossRef] [PubMed]
  27. W. M. Lee and S. H. Yun, “Adaptive aberration correction of GRIN lenses for confocal endomicroscopy,” Opt. Lett.36(23), 4608–4610 (2011).
    [CrossRef] [PubMed]
  28. F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc.5(3), 439–456 (2010).
    [CrossRef] [PubMed]

2013 (1)

J. K. Kim J. W. Choi and S. H. Yun, “350 μm sideview optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt.18, 050502 (2013).
[CrossRef]

2012 (1)

J. K. Kim, W. M. Lee, P. Kim, M. Choi, K. Jung, S. Kim, and S. H. Yun, “Fabrication and operation of GRIN probes for in vivo fluorescence cellular imaging of internal organs in small animals,” Nat. Protoc.7(8), 1456–1469 (2012).
[CrossRef] [PubMed]

2011 (4)

R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
[CrossRef] [PubMed]

A. F. Eichler, E. Chung, D. P. Kodack, J. S. Loeffler, D. Fukumura, and R. K. Jain, “The biology of brain metastases-translation to new therapies,” Nat Rev Clin Oncol8(6), 344–356 (2011).
[PubMed]

E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet, “Cerebrovascular disorders: molecular insights and therapeutic opportunities,” Nat. Neurosci.14(11), 1390–1397 (2011).
[CrossRef] [PubMed]

W. M. Lee and S. H. Yun, “Adaptive aberration correction of GRIN lenses for confocal endomicroscopy,” Opt. Lett.36(23), 4608–4610 (2011).
[CrossRef] [PubMed]

2010 (5)

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc.5(3), 439–456 (2010).
[CrossRef] [PubMed]

M. Fuhrmann, T. Bittner, C. K. E. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms, “Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease,” Nat. Neurosci.13(4), 411–413 (2010).
[CrossRef] [PubMed]

G. Stoll, C. Kleinschnitz, and B. Nieswandt, “Combating innate inflammation: a new paradigm for acute treatment of stroke?” Ann. N. Y. Acad. Sci.1207(1), 149–154 (2010).
[CrossRef] [PubMed]

R. Jin, G. Yang, and G. Li, “Inflammatory mechanisms in ischemic stroke: role of inflammatory cells,” J. Leukoc. Biol.87(5), 779–789 (2010).
[CrossRef] [PubMed]

G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc.5(2), 201–208 (2010).
[CrossRef] [PubMed]

2009 (5)

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
[CrossRef] [PubMed]

M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
[CrossRef] [PubMed]

T. H. Chia and M. J. Levene, “Microprisms for in vivo multilayer cortical imaging,” J. Neurophysiol.102(2), 1310–1314 (2009).
[CrossRef] [PubMed]

K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
[CrossRef] [PubMed]

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods6(7), 511–512 (2009).
[CrossRef] [PubMed]

2008 (1)

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt.13(1), 010501 (2008).
[CrossRef] [PubMed]

2007 (1)

L. Fu, A. Jain, C. Cranfield, H. K. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt.12(4), 040501 (2007).
[CrossRef] [PubMed]

2006 (2)

T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
[CrossRef] [PubMed]

D. E. Bredesen, R. V. Rao, and P. Mehlen, “Cell death in the nervous system,” Nature443(7113), 796–802 (2006).
[CrossRef] [PubMed]

2005 (3)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods2(12), 932–940 (2005).
[CrossRef] [PubMed]

J. Tilgner, M. Herr, C. Ostertag, and B. Volk, “Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors,” Neurosurgery56(2), 257–265, discussion 257–265 (2005).
[CrossRef] [PubMed]

Y. Chudnovsky, P. A. Khavari, and A. E. Adams, “Melanoma genetics and the development of rational therapeutics,” J. Clin. Invest.115(4), 813–824 (2005).
[PubMed]

2001 (1)

L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
[PubMed]

1999 (1)

I. J. Fidler, G. Schackert, R. D. Zhang, R. Radinsky, and T. Fujimaki, “The biology of melanoma brain metastasis,” Cancer Metastasis Rev.18(3), 387–400 (1999).
[CrossRef] [PubMed]

1997 (1)

A. Hara, M. Niwa, N. Yoshimi, and H. Mori, “Apoptotic cell death in vulnerable subpopulation of cerebellar granule cells,” Acta Neuropathol.94(5), 517–518 (1997).
[CrossRef] [PubMed]

1995 (1)

K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
[CrossRef] [PubMed]

1991 (1)

W. Feiden, U. Steude, K. Bise, and O. Gündisch, “Accuracy of stereotactic brain tumor biopsy: comparison of the histologic findings in biopsy cylinders and resected tumor tissue,” Neurosurg. Rev.14(1), 51–56 (1991).
[PubMed]

Adamantidis, A. R.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc.5(3), 439–456 (2010).
[CrossRef] [PubMed]

Adams, A. E.

Y. Chudnovsky, P. A. Khavari, and A. E. Adams, “Melanoma genetics and the development of rational therapeutics,” J. Clin. Invest.115(4), 813–824 (2005).
[PubMed]

Airan, R. D.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc.5(3), 439–456 (2010).
[CrossRef] [PubMed]

Akagi, H.

K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
[CrossRef] [PubMed]

Arumugam, T. V.

M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
[CrossRef] [PubMed]

T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
[CrossRef] [PubMed]

Assaf, Y.

L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
[PubMed]

Attardo, A.

R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
[CrossRef] [PubMed]

Barretto, R. P.

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods6(7), 511–512 (2009).
[CrossRef] [PubMed]

Barretto, R. P. J.

R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
[CrossRef] [PubMed]

Behrens, D.

M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
[CrossRef] [PubMed]

Beni-Adani, L.

L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
[PubMed]

Bise, K.

W. Feiden, U. Steude, K. Bise, and O. Gündisch, “Accuracy of stereotactic brain tumor biopsy: comparison of the histologic findings in biopsy cylinders and resected tumor tissue,” Neurosurg. Rev.14(1), 51–56 (1991).
[PubMed]

Bittner, T.

M. Fuhrmann, T. Bittner, C. K. E. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms, “Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease,” Nat. Neurosci.13(4), 411–413 (2010).
[CrossRef] [PubMed]

Bonhoeffer, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
[CrossRef] [PubMed]

Boyer, L.

K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
[CrossRef] [PubMed]

Bredesen, D. E.

D. E. Bredesen, R. V. Rao, and P. Mehlen, “Cell death in the nervous system,” Nature443(7113), 796–802 (2006).
[CrossRef] [PubMed]

Brenneman, D. E.

L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
[PubMed]

Burgold, S.

M. Fuhrmann, T. Bittner, C. K. E. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms, “Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease,” Nat. Neurosci.13(4), 411–413 (2010).
[CrossRef] [PubMed]

Capps, G.

R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
[CrossRef] [PubMed]

Carmeliet, P.

E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet, “Cerebrovascular disorders: molecular insights and therapeutic opportunities,” Nat. Neurosci.14(11), 1390–1397 (2011).
[CrossRef] [PubMed]

Carson, C. T.

K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
[CrossRef] [PubMed]

Chan, S. L.

T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
[CrossRef] [PubMed]

Cheng, A.

T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
[CrossRef] [PubMed]

Chia, T. H.

T. H. Chia and M. J. Levene, “Microprisms for in vivo multilayer cortical imaging,” J. Neurophysiol.102(2), 1310–1314 (2009).
[CrossRef] [PubMed]

Chigurupati, S.

T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
[CrossRef] [PubMed]

Choe, C. U.

M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
[CrossRef] [PubMed]

Choi, M.

J. K. Kim, W. M. Lee, P. Kim, M. Choi, K. Jung, S. Kim, and S. H. Yun, “Fabrication and operation of GRIN probes for in vivo fluorescence cellular imaging of internal organs in small animals,” Nat. Protoc.7(8), 1456–1469 (2012).
[CrossRef] [PubMed]

Chow, D. K.

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T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
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M. Fuhrmann, T. Bittner, C. K. E. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms, “Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease,” Nat. Neurosci.13(4), 411–413 (2010).
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A. Hara, M. Niwa, N. Yoshimi, and H. Mori, “Apoptotic cell death in vulnerable subpopulation of cerebellar granule cells,” Acta Neuropathol.94(5), 517–518 (1997).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
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T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
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K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
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G. Stoll, C. Kleinschnitz, and B. Nieswandt, “Combating innate inflammation: a new paradigm for acute treatment of stroke?” Ann. N. Y. Acad. Sci.1207(1), 149–154 (2010).
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A. Hara, M. Niwa, N. Yoshimi, and H. Mori, “Apoptotic cell death in vulnerable subpopulation of cerebellar granule cells,” Acta Neuropathol.94(5), 517–518 (1997).
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K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
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T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
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J. Tilgner, M. Herr, C. Ostertag, and B. Volk, “Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors,” Neurosurgery56(2), 257–265, discussion 257–265 (2005).
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T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
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G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc.5(2), 201–208 (2010).
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G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc.5(2), 201–208 (2010).
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K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
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K. Saijo, B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass, “A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death,” Cell137(1), 47–59 (2009).
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K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
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I. J. Fidler, G. Schackert, R. D. Zhang, R. Radinsky, and T. Fujimaki, “The biology of melanoma brain metastasis,” Cancer Metastasis Rev.18(3), 387–400 (1999).
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R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
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L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
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L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R. A. Steingart, D. E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami, “A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice,” J. Pharmacol. Exp. Ther.296(1), 57–63 (2001).
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E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet, “Cerebrovascular disorders: molecular insights and therapeutic opportunities,” Nat. Neurosci.14(11), 1390–1397 (2011).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
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T. V. Arumugam, S. L. Chan, D. G. Jo, G. Yilmaz, S. C. Tang, A. Cheng, M. Gleichmann, E. Okun, V. D. Dixit, S. Chigurupati, M. R. Mughal, X. Ouyang, L. Miele, T. Magnus, S. Poosala, D. N. Granger, and M. P. Mattson, “Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke,” Nat. Med.12(6), 621–623 (2006).
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J. Tilgner, M. Herr, C. Ostertag, and B. Volk, “Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors,” Neurosurgery56(2), 257–265, discussion 257–265 (2005).
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M. Gelderblom, F. Leypoldt, K. Steinbach, D. Behrens, C. U. Choe, D. A. Siler, T. V. Arumugam, E. Orthey, C. Gerloff, E. Tolosa, and T. Magnus, “Temporal and spatial dynamics of cerebral immune cell accumulation in stroke,” Stroke40(5), 1849–1857 (2009).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc.4(8), 1128–1144 (2009).
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K. Nagashima, Y. Fujii, T. Tsukamoto, S. Nukuzuma, M. Satoh, M. Fujita, Y. Fujioka, and H. Akagi, “Apoptotic process of cerebellar degeneration in experimental methylmercury intoxication of rats,” Acta Neuropathol.91(1), 72–77 (1995).
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E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet, “Cerebrovascular disorders: molecular insights and therapeutic opportunities,” Nat. Neurosci.14(11), 1390–1397 (2011).
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J. Tilgner, M. Herr, C. Ostertag, and B. Volk, “Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors,” Neurosurgery56(2), 257–265, discussion 257–265 (2005).
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R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med.17(2), 223–228 (2011).
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A. Hara, M. Niwa, N. Yoshimi, and H. Mori, “Apoptotic cell death in vulnerable subpopulation of cerebellar granule cells,” Acta Neuropathol.94(5), 517–518 (1997).
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Ann. N. Y. Acad. Sci. (1)

G. Stoll, C. Kleinschnitz, and B. Nieswandt, “Combating innate inflammation: a new paradigm for acute treatment of stroke?” Ann. N. Y. Acad. Sci.1207(1), 149–154 (2010).
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Figures (6)

Fig. 1
Fig. 1

(a) Photographs of a side-view probe. The bright area at the center of the prism is due to the illumination light coupled into the probe at the proximal end (not shown). (b) A fabricated needle probe. Inset, a schematic showing focused laser light (blue).

Fig. 2
Fig. 2

Longitudinal monitoring of neuronal cell death in intoxication models. (a) Schematic of FNIB of the cerebellum (blue) with a 22-gauge needle-assisted probe is drawn here. (b) Images of Thy1-YFP cells at days 0, 15, and 30 in a control mouse. (c) Images of Thy1-YFP cells in a mouse treated with methyl mercury. (d) Images of Thy1-YFP cells in a mouse treated with trimethyltin hydroxide(TMT). The images in (b-d) were obtained at 500-1000 µm below the cortical surface of the cerebellum. (e) The changes in cell density over time acrossthe three treatment groups are plotted here. **, P<0.01 (f) The neurological severity scores(NSS) measured for three animal groups (n = 5 each).

Fig. 3
Fig. 3

Visualizing immune cells in a stroke model. (a) Biopsy sites (red dots) in both hemispheres of the brain after occlusion and reperfusion of the right middle cerebral artery. (b) Images of MHC-Class-II + GFP + cells at Days 0, 1, and 3 in the right and left hemispheres. Scale bars, 100 μm. (c) The numbers of MHC-Class-II-GFP cells over time. There is a significant increase of GFP + cells in the right hemisphere. **, P<0.01; ***, P<0.001.

Fig. 4
Fig. 4

Assessing the brain metastasis of melanoma cells. (a) Western blots showing the normal and overexpression levels of p53 for the GFP + and RFP + B16 melanoma cells, respectively. (b) An in vitro image of a mixture of equal numbers of the GFP + and RFP + cells.(c) In vivo imaging of the injected melanoma cells in the deep cortex (blue) with the needle probe (arrow). (d) In vivo images of the melanoma cells at 3 days and 6 days after cell injection. (e) The numbers of neuronal cells, calculated per 1μg (0.001 mm3) of tissue, that were determined to be RFP + or GFP + using the side-view optical probe over a 6-day time course. (f) The numbers of irregularly shaped cells in the brain parenchyma are plotted here. Green circles represent the GFP + B16 cells; red squares represent the RFP + B16 cells. Scale bars in b and d, 100 μm. **,P<0.01. Error bars, standard deviation (n = 3).

Fig. 5
Fig. 5

Histological slides of brain sections at 1 hours (left), 7 days (middle), and 15 days (right) after needle insertion. Hematoxylin and eosin (H&E) stains of the cerebellar granular layers show the tissue damage (upper panels). In situ TUNEL (terminal deoxy- nucleotidyl transferase dUTP nick-end labeling) staining shows the apoptotic and necrotic regions across the needle’s path (lower panels). Scale bars, 100 μm.

Fig. 6
Fig. 6

(a) The neurological severity score (NSS) results for mice (n = 3) receiving biopsy in the thalamus (triangles) and cerebrum (circles). (b) NSS results of a mouse receiving FNIB in the cerebellum. In both cases, the procedures were performed on days 0, 14, and 27, respectively.

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