Abstract
Epilepsy is a diverse group of brain disorders mainly defined by recurrent seizures. Precise localization of epileptic activity in the cerebral cortex and subcortical structures is a complex problem that usually requires a host of methods such as electroencephalography (EEG), magnetic resonance imaging (MRI), and positron emission tomography (PET) in clinical studies. From the end of the previous century, optical imaging methods have yielded revolutionary results when applied to all parts of the brain. In this chapter we cover intrinsic optical imaging and voltage-sensitive dye imaging, as well as several other techniques. All optical imaging techniques reflect various physiological processes in brain tissue which are indissolubly related with neuronal processes. While all the discussed imaging methods are applicable to animal models, several of them can also be used in human medicine for clinical studies and diagnostics. The basic principles of optical imaging of intrinsic signal, voltage-sensitive dye imaging, functional near-infrared spectroscopy, photoacoustic and their variations are described, followed by examples of cutting-edge epileptic studies where they have been utilized. In contrast to PET and fMRI, the main limitation of optical imaging is the limited penetration of photons, which allows us to only image cortical structures no deeper than a few tenths of a millimeter. Advantages include high spatial (up to microns) and temporal (up to milliseconds) resolution and relatively low costs. Scientists and clinicians employ a variety of optical imaging technologies to visualize and study the relationship between neurons, glial cells, and blood vessels. In this chapter we present an overview of the current optical approaches used for the in vivo imaging of epileptic seizures.
Abbreviations
- 2-NBDG:
-
2-(N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino)-2-deoxyglucose
- 4-AP:
-
4-aminopyridine
- AAV:
-
adeno-associated virus
- ADK:
-
adenosine kinase
- BCC:
-
bicuculline
- CCD-camera:
-
charge-coupled device
- CT:
-
computed tomography
- DIOSI:
-
dynamic intrinsic optical signal imaging
- EEG:
-
electroencephalogram
- fMRI:
-
functional magnetic resonance imaging
- fNIRS:
-
Functional near-infrared spectroscopy
- GABA:
-
gamma-aminobutyric acid
- GEVI:
-
Genetically encoded fluorescence indicators
- IOS:
-
Intrinsic optical signal
- MRI:
-
magnetic resonance imaging
- OCT:
-
Optical coherence tomography
- OMAG:
-
optical micro-angiography
- PAT:
-
Photoacoustic imaging
- PCX:
-
picrotoxin
- PET:
-
positron emission tomography
- PMT:
-
photomultipliers
- PTZ:
-
pentylenetetrazol
- SPECT:
-
single photon emission tomography
- VSDi:
-
Voltage-sensitive dye imaging
References
Weissinger, F., et al.: Dentate gyrus autonomous ictal activity in the status epilepticus rat model of epilepsy. Brain Res. 1658, 1–10 (2017). https://doi.org/10.1016/j.brainres.2016.12.030
Lapalme-Remis, S., Cascino, G.D.: Imaging for adults with seizures and epilepsy. Contin. Lifelong Learn. Neurol. 22(5), 1451–1479 (2016). https://doi.org/10.1212/CON.0000000000000370
Lenkov, D.N., Volnova, A.B., Pope, A.R.D., Tsytsarev, V.: Advantages and limitations of brain imaging methods in the research of absence epilepsy in humans and animal models. J. Neurosci. Methods. 212(2) (2013). https://doi.org/10.1016/j.jneumeth.2012.10.018
Yoo, P.E., et al.: 7T-fMRI: faster temporal resolution yields optimal BOLD sensitivity for functional network imaging specifically at high spatial resolution. NeuroImage. 164, 214–229 (2018). https://doi.org/10.1016/j.neuroimage.2017.03.002
Glover, G.H.: Overview of functional magnetic resonance imaging. Neurosurg. Clin. N. Am. 22(2). NIH Public Access, 133–139 (2011). https://doi.org/10.1016/j.nec.2010.11.001
Shi, Y., Zhang, X., Yang, C., Ren, J., Li, Z., Wang, Q.: A review on epileptic foci localization using resting-state functional magnetic resonance imaging. Math. Biosci. Eng. 17(3), 2496–2515 (2020). https://doi.org/10.3934/mbe.2020137
Ghaffari-Rafi, A., Leon-Rojas, J.: Investigatory pathway and principles of patient selection for epilepsy surgery candidates: a systematic review. BMC Neurol. 20(1) (2020). https://doi.org/10.1186/s12883-020-01680-w
Hill, D.K., Keynes, R.D.: Opacity changes in stimulated nerve. J. Physiol. 108(3), 278–281 (1949). https://doi.org/10.1113/jphysiol.1949.sp004331
Zijlmans, M., Zweiphenning, W., van Klink, N.: Changing concepts in presurgical assessment for epilepsy surgery. Nat. Rev. Neurol. 15(10), 594–606 (2019). https://doi.org/10.1038/s41582-019-0224-y
Grinvald, A., Lieke, E., Frostig, R.D., Gilbert, C.D., Wiesel, T.N.: Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature. 324(6095), 361–364 (1986). https://doi.org/10.1038/324361a0
Gratton, G., Chiarelli, A.M., Fabiani, M.: From brain to blood vessels and back: a noninvasive optical imaging approach. Neurophotonics. 4(3), 031208 (2017). https://doi.org/10.1117/1.NPh.4.3.031208
Grinvald, A., et al.: In-vivo optical imaging of cortical architecture and dynamics. In: Modern Techniques in Neuroscience Research, pp. 893–969. Springer, Berlin/Heidelberg (1999)
Lieke, E.E., Frostig, R.D., Arieli, A., Ts’o, D.Y., Hildesheim, R., Grinvald, A.: Optical imaging of cortical activity: real-time imaging using extrinsic dye-signals and high resolution imaging based on slow intrinsic-signals. Annu. Rev. Physiol. 51(1), 543–559 (1989). https://doi.org/10.1146/annurev.ph.51.030189.002551
Frostig, R.D., Lieke, E.E., Ts’o, D.Y., Grinvald, A.: Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc. Natl. Acad. Sci. U. S. A. 87(16), 6082–6086 (1990). https://doi.org/10.1073/pnas.87.16.6082
Grinvald, A., Shoham, D., Shmuel, A., Glaser, D., Vanzetta, I., Shtoyerman, E., Slovin, H., Sterkin, A., Wijnbergen, C., Hildesheim, R., Arieli, A.: In vivo optical imaging of cortical architecture and dynamics. The Grodetsky Center for Research of Higher Brain Functions, The Weizmann Institute of Science Technical Report GC-AG/99-6
Guevara, E., Pouliot, P., Nguyen, D.K., Lesage, F.: Optical imaging of acute epileptic networks in mice. J. Biomed. Opt. 18(7), 076021 (2013). https://doi.org/10.1117/1.JBO.18.7.076021
Zhao, M., Ma, H., Suh, M., Schwartz, T.H.: Spatiotemporal dynamics of perfusion and oximetry during ictal discharges in the rat neocortex. J. Neurosci. 29(9), 2814–2823 (2009). https://doi.org/10.1523/JNEUROSCI.4667-08.2009
Ma, H., Zhao, M., Suh, M., Schwartz, T.H.: Hemodynamic surrogates for excitatory membrane potential change during interictal epileptiform events in rat neocortex. J. Neurophysiol. 101(5), 2550–2562 (2009). https://doi.org/10.1152/jn.90694.2008
Ma, H., et al.: Wide-field in vivo neocortical calcium dye imaging using a convection-enhanced loading technique combined with simultaneous multiwavelength imaging of voltage-sensitive dyes and hemodynamic signals. Neurophotonics. 1(1), 015003 (2014). https://doi.org/10.1117/1.NPh.1.1.015003
Wang, R.K., Subhash, H.M.: Optical microangiography: theory and application. In: Leahy, M.J. (ed.) Microcirculation Imaging. Wiley-VCH Verlag GmbH & Co. KGaA (2012). https://doi.org/10.1002/9783527651238. ISBN:9783527328949
Chander, B.S., Chakravarthy, V.S.: A computational model of neuro-glio-vascular loop interactions. PLoS One. 7(11), e48802 (2012). https://doi.org/10.1371/journal.pone.0048802
Shen, H.-Y., et al.: Overexpression of adenosine kinase in cortical astrocytes and focal neocortical epilepsy in mice. J. Neurosurg. 120(3), 628–638 (2014). https://doi.org/10.3171/2013.10.JNS13918
Jia, Y., Grafe, M.R., Gruber, A., Alkayed, N.J., Wang, R.K.: In vivo optical imaging of revascularization after brain trauma in mice. Microvasc. Res. 81(1), 73–80 (2011). https://doi.org/10.1016/j.mvr.2010.11.003
Sirpal, P., Kassab, A., Pouliot, P., Nguyen, D.K., Lesage, F.: fNIRS improves seizure detection in multimodal EEG-fNIRS recordings. J. Biomed. Opt. 24(05), 1 (2019). https://doi.org/10.1117/1.JBO.24.5.051408
Rizki, E.E., et al.: Determination of epileptic focus side in mesial temporal lobe epilepsy using long-term noninvasive fNIRS/EEG monitoring for presurgical evaluation. Neurophotonics. 2(2), 025003 (2015). https://doi.org/10.1117/1.nph.2.2.025003
Pouliot, P., et al.: Nonlinear hemodynamic responses in human epilepsy: a multimodal analysis with fNIRS-EEG and fMRI-EEG. J. Neurosci. Methods. 204(2), 326–340 (2012). https://doi.org/10.1016/j.jneumeth.2011.11.016
Yang, H., Zhang, T., Zhou, J., Carney, P.R., Jiang, H.: In vivo imaging of epileptic foci in rats using a miniature probe integrating diffuse optical tomography and electroencephalographic source localization. Epilepsia. 56(1), 94–100 (2015). https://doi.org/10.1111/epi.12880
Taraschenko, O., et al.: A mouse model of seizures in anti- N -methyl- d -aspartate receptor encephalitis. Epilepsia. 60(3), 452–463 (2019). https://doi.org/10.1111/epi.14662
Bai, R., Stewart, C.V., Plenz, D., Basser, P.J.: Assessing the sensitivity of diffusion MRI to detect neuronal activity directly. Proc. Natl. Acad. Sci. 113(12), E1728–E1737 (2016). https://doi.org/10.1073/pnas.1519890113
Wang, X., Xie, X., Ku, G., Wang, L.V., Stoica, G.: Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography. J. Biomed. Opt. 11(2), 024015 (2006). https://doi.org/10.1117/1.2192804
Xia, J., Yao, J., Wang, L.V.: Photoacoustic tomography: principles and advances. Electromagn. Waves (Cambridge, Mass.). 147, 1–22 (2014). Accessed 02 Dec 2018. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/25642127
Yao, J., Maslov, K.I., Shi, Y., Taber, L.A., Wang, L.V.: In vivo photoacoustic imaging of transverse blood flow by using Doppler broadening of bandwidth. Opt. Lett. 35(9), 1419 (2010). https://doi.org/10.1364/ol.35.001419
van den Berg, P.J., Daoudi, K., Steenbergen, W.: Review of photoacoustic flow imaging: its current state and its promises. Photoacoustics. 3(3). Elsevier GmbH, 89–99 (2015). https://doi.org/10.1016/j.pacs.2015.08.001
Wang, L.V., Gao, L.: Photoacoustic microscopy and computed tomography: from bench to bedside. Annu. Rev. Biomed. Eng. 16(1), 155–185 (2014). https://doi.org/10.1146/annurev-bioeng-071813-104553
Ning, B., et al.: Ultrasound-aided multi-parametric photoacoustic microscopy of the mouse brain. Sci. Rep. 5(1), 18775 (2015). https://doi.org/10.1038/srep18775
Tsytsarev, V., Rao, B., Maslov, K.I., Li, L., Wang, L.V.: Photoacoustic and optical coherence tomography of epilepsy with high temporal and spatial resolution and dual optical contrasts. J. Neurosci. Methods. 216(2), 142–145 (2013). https://doi.org/10.1016/j.jneumeth.2013.04.001
Gottschalk, S., Fehm, T.F., Deán-Ben, X.L., Razansky, D.: Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography. J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015). https://doi.org/10.1038/jcbfm.2014.249
Baba, H., et al.: Auditory cortical field coding long-lasting tonal offsets in mice. Sci. Rep. 6(1), 34421 (2016). https://doi.org/10.1038/srep34421
Xi, L., Jin, T., Zhou, J., Carney, P., Jiang, H.: Hybrid photoacoustic and electrophysiological recording of neurovascular communications in freely-moving rats. NeuroImage. 161, 232–240 (2017). https://doi.org/10.1016/j.neuroimage.2017.08.037
Satomura, Y., Seki, J., Ooi, Y., Yanagida, T., Seiyama, A.: In vivo imaging of the rat cerebral microvessels with optical coherence tomography. Clin. Hemorheol. Microcirc. 31(1), 31–40 (2004). Accessed 08 Dec 2018. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/15272151
Aguirre, A.D., Chen, Y., Fujimoto, J.G., Ruvinskaya, L., Devor, A., Boas, D.A.: Depth-resolved imaging of functional activation in the rat cerebral cortex using optical coherence tomography. Opt. Lett. 31(23), 3459–3461 (2006). Accessed 08 Dec 2018. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/17099749
Guo, H., et al.: Intravital imaging of adriamycin-induced renal pathology using two-photon microscopy and optical coherence tomography. J. Innov. Opt. Health Sci., 1850030 (2018). https://doi.org/10.1142/S179354581850030X
Leitgeb, R.A., Werkmeister, R.M., Blatter, C., Schmetterer, L.: Doppler optical coherence tomography. Prog. Retin. Eye Res. 41(100), 26–43 (2014). https://doi.org/10.1016/j.preteyeres.2014.03.004
Carmignoto, G., Haydon, P.G.: Astrocyte calcium signaling and epilepsy. Glia. 60(8), 1227–1233 (2012). https://doi.org/10.1002/glia.22318
Gómez-Gonzalo, M., et al.: Ictal but not interictal epileptic discharges activate astrocyte endfeet and elicit cerebral arteriole responses. Front. Cell. Neurosci. 5 (2011). https://doi.org/10.3389/fncel.2011.00008
Mazhar, F., Malhi, S.M., Simjee, S.U.: Comparative studies on the effects of clinically used anticonvulsants on the oxidative stress biomarkers in pentylenetetrazole-induced kindling model of epileptogenesis in mice. J. Basic Clin. Physiol. Pharmacol. 28(1), 31–42 (2017). https://doi.org/10.1515/jbcpp-2016-0034
Haglund, M.M., Ojemann, G.A., Hochman, D.W.: Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature. 358(6388), 668–671 (1992). https://doi.org/10.1038/358668a0
Zhang, C., et al.: Astrocytic endfoot Ca2+ correlates with parenchymal vessel responses during 4-AP induced epilepsy: an in vivo two-photon lifetime microscopy study. J. Cereb. Blood Flow Metab. 39(2), 260–271 (2019). https://doi.org/10.1177/0271678X17725417
Folbergrová, J., Ingvar, M., Siesjö, B.K.: Metabolic changes in cerebral cortex, hippocampus, and cerebellum during sustained bicuculline-induced seizures. J. Neurochem. 37(5), 1228–1238 (1981). Accessed 21 May 2019. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/7299397
Kim, J.H., Khan, R., Thompson, J.K., Ress, D.: Model of the transient neurovascular response based on prompt arterial dilation. J. Cereb. Blood Flow Metab. 33(9), 1429–1439 (2013). https://doi.org/10.1038/jcbfm.2013.90
Zhao, M., Suh, M., Ma, H., Perry, C., Geneslaw, A., Schwartz, T.H.: Focal increases in perfusion and decreases in hemoglobin oxygenation precede seizure onset in spontaneous human epilepsy. Epilepsia. 48(11), 2059–2067 (2007). https://doi.org/10.1111/j.1528-1167.2007.01229.x
Baird-Daniel, E., et al.: Glial calcium waves are triggered by seizure activity and not essential for initiating ictal onset or neurovascular coupling. Cereb. Cortex. 27(6), 3318–3330 (2017). https://doi.org/10.1093/cercor/bhx072
Wylęgała, A.: Principles of OCTA and applications in clinical neurology. Curr. Neurol. Neurosci. Rep. 18(12), 96 (2018). https://doi.org/10.1007/s11910-018-0911-x
Daniel, A.G.S., Laffont, P., Zhao, M., Ma, H., Schwartz, T.H.: Optical electrocorticogram (OECoG) using wide-field calcium imaging reveals the divergence of neuronal and glial activity during acute rodent seizures. Epilepsy Behav. 49, 61–65 (2015). https://doi.org/10.1016/j.yebeh.2015.04.036
López-Bendito, G.: Development of the thalamocortical interactions: past, present and future. Neuroscience. 385, 67–74 (2018). https://doi.org/10.1016/j.neuroscience.2018.06.020
Song, Y., et al.: Intraoperative optical mapping of epileptogenic cortices during non-ictal periods in pediatric patients. NeuroImage Clin. 11, 423–434 (2016). https://doi.org/10.1016/j.nicl.2016.02.015
Sato, K., Nariai, T., Momose-Sato, Y., Kamino, K.: Intraoperative intrinsic optical imaging of human somatosensory cortex during neurosurgical operations. Neurophotonics. 4(3), 031205 (2016). https://doi.org/10.1117/1.NPh.4.3.031205
Rayshubskiy, A., et al.: Direct, intraoperative observation of ∼0.1 Hz hemodynamic oscillations in awake human cortex: implications for fMRI. NeuroImage. 87, 323–331 (2014). https://doi.org/10.1016/j.neuroimage.2013.10.044
Sobottka, S.B., et al.: Intraoperative optical imaging of intrinsic signals: a reliable method for visualizing stimulated functional brain areas during surgery. J. Neurosurg. 119(4), 853–863 (2013). https://doi.org/10.3171/2013.5.JNS122155
Buxton, R.B., Uludağ, K., Dubowitz, D.J., Liu, T.T.: Modeling the hemodynamic response to brain activation. NeuroImage. 23, S220–S233 (2004). https://doi.org/10.1016/j.neuroimage.2004.07.013
Buxton, R.B., Frank, L.R.: A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J. Cereb. Blood Flow Metab. 17(1), 64–72 (1997). https://doi.org/10.1097/00004647-199701000-00009
Devor, A., et al.: “Overshoot” of O2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels. J. Neurosci. 31(38), 13676–13681 (2011). https://doi.org/10.1523/JNEUROSCI.1968-11.2011
Cannestra, A.F., Pouratian, N., Forage, J., Bookheimer, S.Y., Martin, N.A., Toga, A.W.: Functional magnetic resonance imaging and optical imaging for dominant-hemisphere perisylvian arteriovenous malformations. Neurosurgery. 55(4), 804–814 (2004). https://doi.org/10.1227/01.NEU.0000137654.27826.71
Toga, A.W., Cannestra, A.F., Black, K.L.: The temporal/spatial evolution of optical signals in human cortex. Cereb. Cortex. 5(6), 561–565 (1995). https://doi.org/10.1093/cercor/5.6.561
Berwick, J., et al.: Fine detail of neurovascular coupling revealed by spatiotemporal analysis of the hemodynamic response to single whisker stimulation in rat barrel cortex. J. Neurophysiol. 99(2), 787–798 (2008). https://doi.org/10.1152/jn.00658.2007
Ba, A.M., et al.: Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J. Neurophysiol. 88(5), 2726–2735 (2002). https://doi.org/10.1152/jn.00729.2001
Suh, M., Bahar, S., Mehta, A.D., Schwartz, T.H.: Blood volume and hemoglobin oxygenation response following electrical stimulation of human cortex. NeuroImage. 31(1), 66–75 (2006). https://doi.org/10.1016/j.neuroimage.2005.11.030
Suh, M., Bahar, S., Mehta, A.D., Schwartz, T.H.: Temporal dependence in uncoupling of blood volume and oxygenation during interictal epileptiform events in rat neocortex. J. Neurosci. 25(1), 68–77 (2005). https://doi.org/10.1523/JNEUROSCI.2823-04.2005
Bahar, S., Suh, M., Zhao, M., Schwartz, T.H.: Intrinsic optical signal imaging of neocortical seizures: the ‘epileptic dip’. Neuroreport. 17(5), 499–503 (2006). https://doi.org/10.1097/01.wnr.0000209010.78599.f5
Hong, K.-S., Zafar, A.: Existence of initial dip for BCI: an illusion or reality. Front. Neurorobot. 12, 69 (2018). https://doi.org/10.3389/fnbot.2018.00069
Hu, X., Yacoub, E.: The story of the initial dip in fMRI. NeuroImage. 62(2), 1103–1108 (2012). https://doi.org/10.1016/j.neuroimage.2012.03.005
Sheth, S.A., et al.: Columnar specificity of microvascular oxygenation and volume responses: implications for functional brain mapping. J. Neurosci. 24(3), 634–641 (2004). https://doi.org/10.1523/JNEUROSCI.4526-03.2004
Saito, T., et al.: Posterior quadrantectomy for infant with refractory epilepsy: a case report. No Shinkei Geka. 47(3), 349–356 (2019). https://doi.org/10.11477/mf.1436203943
Dunn, A.K., et al.: Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. Opt. Lett. 28(1), 28–30 (2003). Accessed 19 Sep 2018. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/12656525
Vanzetta, I., Grinvald, A.: Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science. 286(5444), 1555–1558 (1999). Accessed 21 May 2019. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/10567261
Ances, B.M.: Coupling of changes in cerebral blood flow with neural activity: what must initially dip must come back up. J. Cereb. Blood Flow Metab. 24(1), 1–6 (2004). https://doi.org/10.1097/01.WCB.0000103920.96801.12
Wang, Z., Hughes, S., Dayasundara, S., Menon, R.S.: Theoretical and experimental optimization of laser speckle contrast imaging for high specificity to brain microcirculation. J. Cereb. Blood Flow Metab. 27(2), 258–269 (2007). https://doi.org/10.1038/sj.jcbfm.9600357
Zaidi, A.D., et al.: Simultaneous epidural functional near-infrared spectroscopy and cortical electrophysiology as a tool for studying local neurovascular coupling in primates. NeuroImage. 120, 394–399 (2015). https://doi.org/10.1016/j.neuroimage.2015.07.019
Lindauer, U., et al.: No evidence for early decrease in blood oxygenation in rat whisker cortex in response to functional activation. NeuroImage. 13(6), 988–1001 (2001). https://doi.org/10.1006/nimg.2000.0709
Tian, P., et al.: Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc. Natl. Acad. Sci. 107(34), 15246–15251 (2010). https://doi.org/10.1073/pnas.1006735107
Takeshita, D., Bahar, S.: Synchronization analysis of voltage-sensitive dye imaging during focal seizures in the rat neocortex. Chaos. 21(4), 047506 (2011). https://doi.org/10.1063/1.3640043
Graebenitz, S., et al.: Directional spread of activity in synaptic networks of the human lateral amygdala. Neuroscience. 349, 330–340 (2017). https://doi.org/10.1016/j.neuroscience.2017.03.009
Kulkarni, R.U., Kramer, D.J., Pourmandi, N., Karbasi, K., Bateup, H.S., Miller, E.W.: Voltage-sensitive rhodol with enhanced two-photon brightness. Proc. Natl. Acad. Sci. 114(11), 2813–2818 (2017). https://doi.org/10.1073/pnas.1610791114
Cappaert, N.L.M., Werkman, T.R., Benito, N., Witter, M.P., Baayen, J.C., Wadman, W.J.: Carbamazepine modulates the spatiotemporal activity in the dentate gyrus of rats and pharmacoresistant humans in vitro. Brain Behav. 6(6), e00463 (2016). https://doi.org/10.1002/brb3.463
Proix, T., Jirsa, V.K., Bartolomei, F., Guye, M., Truccolo, W.: Predicting the spatiotemporal diversity of seizure propagation and termination in human focal epilepsy. Nat. Commun. 9(1) (2018). https://doi.org/10.1038/s41467-018-02973-y
Huang, X., et al.: Spiral waves in disinhibited mammalian neocortex. J. Neurosci. 24(44), 9897–9902 (2004). https://doi.org/10.1523/JNEUROSCI.2705-04.2004
Huang, X., Xu, W., Liang, J., Takagaki, K., Gao, X., Wu, J.: Spiral wave dynamics in neocortex. Neuron. 68(5), 978–990 (2010). https://doi.org/10.1016/j.neuron.2010.11.007
Tang, Q., et al.: 3D mesoscopic imaging of neural connections in sensory and motor cortices. In: 2016 IEEE Photonics Conference, IPC 2016 (2017). https://doi.org/10.1109/IPCon.2016.7831020
Tang, Q., Tsytsarev, V., Frank, A., Wu, Y., Chen, C.W., Erzurumlu, R.S., Chen, Y.: In vivo mesoscopic voltage-sensitive dye imaging of brain activation. Sci. Rep. 6, 25269 (2016). https://doi.org/10.1038/srep25269
Shultz, S.R., O’Brien, T.J., Stefanidou, M., Kuzniecky, R.I.: Neuroimaging the epileptogenic process. Neurotherapeutics. 11(2), 347–357 (2014). https://doi.org/10.1007/s13311-014-0258-1
Guo, Y., et al.: In vivo mapping of temporospatial changes in glucose utilization in rat brain during epileptogenesis: an 18F-fluorodeoxyglucose-small animal positron emission tomography study. Neuroscience. 162(4), 972–979 (2009). https://doi.org/10.1016/j.neuroscience.2009.05.041
Tsytsarev, V., Maslov, K.I., Yao, J., Parameswar, A.R., Demchenko, A.V., Wang, L.V.: In vivo imaging of epileptic activity using 2-NBDG, a fluorescent deoxyglucose analog. J. Neurosci. Methods. 203(1) (2012). https://doi.org/10.1016/j.jneumeth.2011.09.005
Yao, J., et al.: Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo. In: Photons Plus Ultrasound: Imaging and Sensing Progress in Biomedical Optics and Imaging – Proceedings of SPIE, vol. 8581. SPIE, Bellingham (2013). https://doi.org/10.1117/12.2005645
Santhakumar, H., et al.: Real time imaging and dynamics of hippocampal Zn2+ under epileptic condition using a ratiometric fluorescent probe. Sci. Rep. 8(1), 9069 (2018). https://doi.org/10.1038/s41598-018-27029-5
Rossi, L.F., Kullmann, D.M., Wykes, R.C.: The enlightened brain: novel imaging methods focus on epileptic networks at multiple scales. Front. Cell. Neurosci. 12, 82 (2018). https://doi.org/10.3389/fncel.2018.00082
Takao, T., et al.: Transcranial imaging of audiogenic epileptic foci in the cortex of DBA/2J mice. Neuroreport. 17(3), 267–271 (2006). https://doi.org/10.1097/01.wnr.0000201505.61373.42
Suh, M., Shariff, S., Bahar, S., Mehta, A.D., Schwartz, T.H.: Intrinsic optical signal imaging of normal and abnormal physiology in animals and humans--seeing the invisible. Clin. Neurosurg. 52, 135–149 (2005). Accessed 07 July 2018. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/16626065
Kitaura, H., Kakita, A.: Optical imaging of human epileptogenic tissues in vitro. Neuropathology. 33(4), 469–474 (2013). https://doi.org/10.1111/neup.12017
Michael, N., Bischof, H.-J., Löwel, S.: Flavoprotein autofluorescence imaging of visual system activity in zebra finches and mice. PLoS One. 9(1), e85225 (2014). https://doi.org/10.1371/journal.pone.0085225
Kwon, S.E., Tsytsarev, V., Erzurumlu, R.S., O’Connor, D.H.: Organization of orientation-specific whisker deflection responses in layer 2/3 of mouse somatosensory cortex. Neuroscience. 368, 46–56 (2018). https://doi.org/10.1016/J.NEUROSCIENCE.2017.07.067
Tsukano, H., Horie, M., Takahashi, K., Hishida, R., Takebayashi, H., Shibuki, K.: Independent tonotopy and thalamocortical projection patterns in two adjacent parts of the classical primary auditory cortex in mice. Neurosci. Lett. 637, 26–30 (2017). https://doi.org/10.1016/j.neulet.2016.11.062
Tohmi, M., Takahashi, K., Kubota, Y., Hishida, R., Shibuki, K.: Transcranial flavoprotein fluorescence imaging of mouse cortical activity and plasticity. J. Neurochem. 109, 3–9 (2009). https://doi.org/10.1111/j.1471-4159.2009.05926.x
Nakai, J., Ohkura, M., Imoto, K.: A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol. 19(2), 137–141 (2001). https://doi.org/10.1038/84397
Miyawaki, A., et al.: Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin. Nature. 388(6645), 882–887 (1997). https://doi.org/10.1038/42264
Lin, M.Z., Schnitzer, M.J.: Genetically encoded indicators of neuronal activity. Nat. Neurosci. 19(9), 1142–1153 (2016). https://doi.org/10.1038/nn.4359
Peterka, D.S., Takahashi, H., Yuste, R.: Imaging voltage in neurons. Neuron. 69(1), 9–21 (2011). https://doi.org/10.1016/j.neuron.2010.12.010
Yang, H.H., St-Pierre, F.: Genetically encoded voltage indicators: opportunities and challenges. J. Neurosci. 36(39), 9977–9989 (2016). https://doi.org/10.1523/JNEUROSCI.1095-16.2016
Grienberger, C., Konnerth, A.: Imaging calcium in neurons. Neuron. 73(5), 862–885 (2012). https://doi.org/10.1016/j.neuron.2012.02.011
Paredes, J.M., et al.: Synchronous bioimaging of intracellular pH and chloride based on LSS fluorescent protein. ACS Chem. Biol. 11(6), 1652–1660 (2016). https://doi.org/10.1021/acschembio.6b00103
Kannan, M., Vasan, G., Pieribone, V.A.: Optimizing strategies for developing genetically encoded voltage indicators. Front. Cell. Neurosci. 13. Frontiers Media S.A., 1–17 (2019). https://doi.org/10.3389/fncel.2019.00053
Sepehri Rad, M., et al.: Voltage and calcium imaging of brain activity. Biophys. J. 113(10), 2160–2167 (2017). https://doi.org/10.1016/j.bpj.2017.09.040
Bando, Y., Grimm, C., Cornejo, V.H., Yuste, R.: Genetic voltage indicators. BMC Biol. 17(1), 1–12 (2019). https://doi.org/10.1186/s12915-019-0682-0
Storace, D., Sepehri Rad, M., Kang, B., Cohen, L.B., Hughes, T., Baker, B.J.: Toward better genetically encoded sensors of membrane potential. Trends Neurosci. 39(5), 277–289 (2016). https://doi.org/10.1016/j.tins.2016.02.005
Madisen, L., et al.: Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron. 85(5), 942–958 (2015). https://doi.org/10.1016/j.neuron.2015.02.022
Barretto, R.P.J., Schnitzer, M.J.: In vivo optical microendoscopy for imaging cells lying deep within live tissue. Cold Spring Harb. Protoc. (10), pdb.top071464 (2012, 2012). https://doi.org/10.1101/pdb.top071464
Barretto, R.P.J., et al.: Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nat. Med. 17(2), 223–228 (2011). https://doi.org/10.1038/nm.2292
Flusberg, B.A., et al.: High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods. 5(11), 935–938 (2008). https://doi.org/10.1038/nmeth.1256
Tang, Q., Tsytsarev, V., Liang, C.-P., Akkentli, F., Erzurumlu, R.S., Chen, Y.: In vivo voltage-sensitive dye imaging of subcortical brain function. Sci. Rep. 5, 17325 (2015). https://doi.org/10.1038/srep17325
Raimondo, J.V., et al.: Tight coupling of astrocyte pH dynamics to epileptiform activity revealed by genetically encoded pH sensors. J. Neurosci. 36(26), 7002–7013 (2016). https://doi.org/10.1523/JNEUROSCI.0664-16.2016
Mcallister, A.K.: Biolistic transfection of neurons materials recipes notes and remarks references introduction. Plasmid. 3524, 1–13 (2000). https://doi.org/10.1126/stke.2000.51.pl1
Cela, E., et al.: An optogenetic kindling model of neocortical epilepsy. Sci. Rep. 9(1), 1–12 (2019). https://doi.org/10.1038/s41598-019-41533-2
Löscher, W.: Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs. Seizure. 20(5), 359–368 (2011). https://doi.org/10.1016/j.seizure.2011.01.003
Stafstrom, C.E., Moshé, S.L., Swann, J.W., Nehlig, A., Jacobs, M.P., Schwartzkroin, P.A.: Models of pediatric epilepsies: strategies and opportunities. Epilepsia. 47(8), 1407–1414 (2006). https://doi.org/10.1111/j.1528-1167.2006.00674_1.x
Kandratavicius, L., et al.: Animal models of epilepsy: use and limitations. Neuropsychiatr. Dis. Treat. 10, 1693–1705 (2014). https://doi.org/10.2147/NDT.S50371
Turrini, L., et al.: Optical mapping of neuronal activity during seizures in zebrafish. Sci. Rep. 7(1), 3025 (2017). https://doi.org/10.1038/s41598-017-03087-z
Wenzel, M., Hamm, J.P., Peterka, D.S., Yuste, R.: Reliable and elastic propagation of cortical seizures in vivo. Cell Rep. 19(13), 2681–2693 (2017). https://doi.org/10.1016/j.celrep.2017.05.090
Abraham, T., Feng, J.: Evolution of brain imaging instrumentation. Semin. Nucl. Med. 41(3), 202–219 (2011). https://doi.org/10.1053/j.semnuclmed.2010.12.001
Lo, F.-S., Erzurumlu, R.S.: Insulin receptor sensitization restores neocortical excitation/inhibition balance in a mouse model of autism. Mol. Autism. 9(1), 13 (2018). https://doi.org/10.1186/s13229-018-0196-6
Pavone, P., Striano, P., Falsaperla, R., Pavone, L., Ruggieri, M.: Infantile spasms syndrome, West syndrome and related phenotypes: what we know in 2013. Brain Dev. 36(9), 739–751 (2014). https://doi.org/10.1016/j.braindev.2013.10.008
Ho, A.L., Salib, A.-M.N., Pendharkar, A.V., Sussman, E.S., Giardino, W.J., Halpern, C.H.: The nucleus accumbens and alcoholism: a target for deep brain stimulation. Neurosurg. Focus. 45(2), E12 (2018). https://doi.org/10.3171/2018.5.FOCUS18157
Miyakawa, N., Yazawa, I., Sasaki, S., Momose-Sato, Y., Sato, K.: Optical analysis of acute spontaneous epileptiform discharges in the in vivo rat cerebral cortex. NeuroImage. 18(3), 622–632 (2003). Accessed 19 May 2019. [Online]. Available: http://www.ncbi.nlm.nih.gov/pubmed/12667839
Serikawa, T., Mashimo, T., Kuramoto, T., Voigt, B., Ohno, Y., Sasa, M.: Advances on genetic rat models of epilepsy. Exp. Anim. 64(1), 1–17 (2015). https://doi.org/10.1538/expanim.14-0066
Yang, F., Yang, L., Wataya-Kaneda, M., Teng, L., Katayama, I.: Epilepsy in a melanocyte-lineage mTOR hyperactivation mouse model: a novel epilepsy model. PLoS One. 15(1), 1–18 (2020). https://doi.org/10.1371/journal.pone.0228204
Chen, Y., et al.: Integrated optical coherence tomography (OCT) and fluorescence laminar optical tomography (FLOT) for depth-resolved subsurface cancer imaging. In: Biomedical Optics and 3-D Imaging, p. BSuD9 (2010). https://doi.org/10.1364/BIOMED.2010.BSuD9
Chen, Y., Aguirre, A.D., Ruvinskaya, L., Devor, A., Boas, D.A., Fujimoto, J.G.: Optical coherence tomography (OCT) reveals depth-resolved dynamics during functional brain activation. J. Neurosci. Methods. 178(1), 162–173 (2009). https://doi.org/10.1016/j.jneumeth.2008.11.026
Obrenovitch, T.P., Chen, S., Farkas, E.: Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. NeuroImage. 45(1), 68–74 (2009). https://doi.org/10.1016/j.neuroimage.2008.11.025
Kalchenko, V., Sdobnov, A., Meglinski, I., Kuznetsov, Y., Molodij, G., Harmelin, A.: A robust method for adjustment of laser speckle contrast imaging during transcranial mouse brain visualization. Photonics. 6(3), 80 (2019). https://doi.org/10.3390/photonics6030080
Kalchenko, V., Meglinski, I., Sdobnov, A., Kuznetsov, Y., Harmelin, A.: Combined laser speckle imaging and fluorescent intravital microscopy for monitoring acute vascular permeability reaction. J. Biomed. Opt. 24(06), 1 (2019). https://doi.org/10.1117/1.jbo.24.6.060501
Hochbaum, D.R., et al.: All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods. 11(8), 825–833 (2014). https://doi.org/10.1038/nmeth.3000
Zou, P., et al.: Bright and fast multicoloured voltage reporters via electrochromic FRET. Nat. Commun. 5 (2014). https://doi.org/10.1038/ncomms5625
Piatkevich, K.D., et al.: Population imaging of neural activity in awake behaving mice. Nature. 574(7778), 413–417 (2019). https://doi.org/10.1038/s41586-019-1641-1
Bertrand, S.J., et al.: Transient neonatal sleep fragmentation results in long-term neuroinflammation and cognitive impairment in a rabbit model. Exp. Neurol. 327, 113212 (2020). https://doi.org/10.1016/j.expneurol.2020.113212
Kannan, M., et al.: Fast, in vivo voltage imaging using a red fluorescent indicator. Nat. Methods. 15(12), 1108–1116 (2018). https://doi.org/10.1038/s41592-018-0188-7
Abdelfattah, A.S., et al.: Bright and photostable chemigenetic indicators for extended in vivo voltage imaging. Science. 365(6454), 699–704 (2019). https://doi.org/10.1126/science.aav6416
Gong, Y., et al.: High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor. Science (80-.). 350(6266), 1361–1366 (2015). https://doi.org/10.1126/science.aab0810
Abdelfattah, A.S., et al.: A bright and fast red fluorescent protein voltage indicator that reports neuronal activity in organotypic brain slices. J. Neurosci. 36(8), 2458–2472 (2016). https://doi.org/10.1523/JNEUROSCI.3484-15.2016
Akemann, W., Mutoh, H., Perron, A., Park, Y.K., Iwamoto, Y., Knöpfel, T.: Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J. Neurophysiol. 108(8), 2323–2337 (2012). https://doi.org/10.1152/jn.00452.2012
Lee, S., Geiller, T., Jung, A., Nakajima, R., Song, Y.K., Baker, B.J.: Improving a genetically encoded voltage indicator by modifying the cytoplasmic charge composition. Sci. Rep. 7(1), 1–16 (2017). https://doi.org/10.1038/s41598-017-08731-2
Han, Z., Jin, L., Platisa, J., Cohen, L.B., Baker, B.J., Pieribone, V.A.: Fluorescent protein voltage probes derived from ArcLight that respond to membrane voltage changes with fast kinetics. PLoS One. 8(11), 1–9 (2013). https://doi.org/10.1371/journal.pone.0081295
Villette, V., et al.: Ultrafast two-photon imaging of a high-gain voltage indicator in awake behaving mice. Cell. 179(7), 1590–1608.e23 (2019). https://doi.org/10.1016/j.cell.2019.11.004
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Tsytsarev, V. (2022). Optical Imaging of Epileptic Seizures. In: Thakor, N.V. (eds) Handbook of Neuroengineering. Springer, Singapore. https://doi.org/10.1007/978-981-15-2848-4_124-2
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