Direct measurement of neuronal ensemble activity using photoacoustic imaging in the stimulated Fos-LacZ transgenic rat brain: A proof-of-principle study

Haber, 2010, Neurocircuitry: a window into the networks underlying neuropsychiatric disease, Neuropsychopharmacology, 35, 1, 10.1038/npp.2009.146 Heeger, 2002, What does fMRI tell us about neuronal activity?, Nat. Rev. Neurosci., 3, 142, 10.1038/nrn730 White, 2011, Imaging of functional connectivity in the mouse brain, PLoS One, 6, 10.1371/journal.pone.0016322 Nasiriavanaki, 2014, High-resolution photoacoustic tomography of resting-state functional connectivity in the mouse brain, Proc. Natl. Acad. Sci. U. S. A., 111, 21, 10.1073/pnas.1311868111 Chong, 2015, Cerebral metabolic rate of oxygen (CMRO2) assessed by combined Doppler and spectroscopic OCT, Biomed. Opt. Express, 6, 3941, 10.1364/BOE.6.003941 Sato, 2017, Fast varifocal two-photon microendoscope for imaging neuronal activity in the deep brain, Biomed. Opt. Express, 8, 4049, 10.1364/BOE.8.004049 Meng, 2019, High-throughput synapse-resolving two-photon fluorescence microendoscopy for deep-brain volumetric imaging in vivo, eLife, 8, 10.7554/eLife.40805 Jo, 2011, 4 Villringer, 1995, Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging, Cerebrovasc. Brain Metab. Rev., 7, 240 van den Berg, 2015, Review of photoacoustic flow imaging: its current state and its promises, Photoacoustics, 3, 89, 10.1016/j.pacs.2015.08.001 Lv, 2020, In vivo photoacoustic imaging dynamically monitors the structural and functional changes of ischemic stroke at a very early stage, Theranostics, 10, 816, 10.7150/thno.38554 Roshchina, 2018, New approaches to cognitive neurobiology: methods for two-photon in vivo imaging of cognitively active neurons, Neurosci. Behav. Physiol., 48, 741, 10.1007/s11055-018-0625-1 Koya, 2009, Targeted disruption of cocaine-activated accumbens neurons prevents context-specific sensitization, Nat. Neurosci., 12, 1069, 10.1038/nn.2364 Knapska, 2009, Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear, Learn. Mem., 16, 486, 10.1101/lm.1463909 Gunaydin, 2014, Natural neural projection dynamics underlying social behavior, Cell, 157, 1535, 10.1016/j.cell.2014.05.017 Glover, 2011, Overview of functional magnetic resonance imaging, Neurosurg. Clin. N. Am., 22, 133, 10.1016/j.nec.2010.11.001 Gottschalk, 2019, Rapid volumetric optoacoustic imaging of neural dynamics across the mouse brain, Nat. Biomed. Eng., 3, 392, 10.1038/s41551-019-0372-9 Kang, 2019, Transcranial recording of electrophysiological neural activity in the rodent brain in vivo using functional photoacoustic imaging of near-infrared voltage-sensitive dye, Front. Neurosci., 13 Cruz, 2013, New technologies for examining the role of neuronal ensembles in drug addiction and fear, Nat. Rev. Neurosci., 14, 743, 10.1038/nrn3597 Cruz, 2015, Using c-fos to study neuronal ensembles in corticostriatal circuitry of addiction, Brain Res., 1628, 157, 10.1016/j.brainres.2014.11.005 Yao, 2014, Photoacoustic brain imaging: from microscopic to macroscopic scales, Neurophotonics, 1, 10.1117/1.NPh.1.1.011003 Li, 2008, Simultaneous imaging of a lacZ-marked tumor and microvasculature morphology in vivo by dual-wavelength photoacoustic microscopy, J. Innov. Opt. Health Sci., 1, 207, 10.1142/S1793545808000212 Takatani, 1979, Theoretical analysis of diffuse reflectance from a two-layer tissue model, IEEE Trans. Biomed. Eng. BME, 26, 656, 10.1109/TBME.1979.326455 Li, 2007, Photoacoustic imaging of lacZ gene expression in vivo, J. Biomed. Opt., 12, 10.1117/1.2717531 Cepko, 1998, Detection of beta-galactosidase and alkaline phosphatase activities in tissue Grosso, 2018, A neuronal basis for fear discrimination in the lateral amygdala, Nat. Commun., 9, 1214, 10.1038/s41467-018-03682-2 Koya, 2016, Daun02 inactivation of behaviorally activated Fos-expressing neuronal ensembles, Curr. Protoc. Neurosci., 76, 36 Kovács, 1998, Invited review c-Fos as a transcription factor: a stressful (re)view from a functional map, Neurochem. Int., 33, 287, 10.1016/S0197-0186(98)00023-0 Chung, 2015, A brief introduction to the transduction of neural activity into Fos signal, Dev. Reprod., 19, 61, 10.12717/DR.2015.19.2.061 Koya, 2016, Daun02 inactivation of behaviorally-activated Fos-expressing neuronal ensembles, Curr. Protoc. Neurosci., 76, 36 Allen, 2019, Enhanced neuronal and blunted hemodynamic reactivity to cocaine in the prefrontal cortex following extended cocaine access: optical imaging study in anesthetized rats, Addict. Biol., 24, 485, 10.1111/adb.12615 2011 Lojda, 1970, Indigogenic methods for glycosidases, Histochemie, 23, 266, 10.1007/BF00306428 Gould, 2014, Optical-thermal light-tissue interactions during photoacoustic breast imaging, Biomed. Opt. Express, 5, 832, 10.1364/BOE.5.000832 Institute, 2018 Kratkiewicz, 2021, Technical considerations in the Verasonics research ultrasound platform for developing a photoacoustic imaging system, Biomed. Opt. Express, 12, 1050, 10.1364/BOE.415481 Jacques, 2013, Optical properties of biological tissues: a review, Phys. Med. Biol., 58, R37, 10.1088/0031-9155/58/11/R37 Turani, 2019, Optical radiomic signatures derived from optical coherence tomography images to improve identification of melanoma, Cancer Res., 79, 2021, 10.1158/0008-5472.CAN-18-2791 Xiao, 2007, A new coordinate system for rodent brain and variability in the brain weights and dimensions of different ages in the naked mole-rat, J. Neurosci. Methods, 162, 162, 10.1016/j.jneumeth.2007.01.007 Brown, 1992, Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures, J. Neurosci., 12, 4112, 10.1523/JNEUROSCI.12-10-04112.1992 Smith, 1992, Induction of c-fos mRNA in rat brain by conditioned and unconditioned stressors, Brain Res., 578, 135, 10.1016/0006-8993(92)90240-A Kasof, 1995, Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats, J. Neurosci., 15, 4238, 10.1523/JNEUROSCI.15-06-04238.1995 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Bosschaart, 2014, A literature review and novel theoretical approach on the optical properties of whole blood, Lasers Med. Sci., 29, 453, 10.1007/s10103-013-1446-7 Fang, 2009, Monte Carlo simulation of photon migration in 3D turbid media accelerated by graphics processing units, Opt. Express, 17, 20178, 10.1364/OE.17.020178 Bullitt, 1990, Expression of C-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat, J. Comp. Neurol., 296, 517, 10.1002/cne.902960402 Ehret, 1991, Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression, Brain Res., 567, 350, 10.1016/0006-8993(91)90819-H Beck, 1995, Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment, J. Neurosci., 15, 709, 10.1523/JNEUROSCI.15-01-00709.1995 Marie-Claire, 2003, Fos but not Cart (cocaine and amphetamine regulated transcript) is overexpressed by several drugs of abuse: a comparative study using real-time quantitative polymerase chain reaction in rat brain, Neurosci. Lett., 345, 77, 10.1016/S0304-3940(03)00307-0 Everitt, 2002, Psychomotor stimulant addiction: a neural systems perspective, J. Neurosci., 22, 3312, 10.1523/JNEUROSCI.22-09-03312.2002 Koob, 2010, Neurocircuitry of addiction, Neuropsychopharmacology, 35, 217, 10.1038/npp.2009.110 Nestler, 2001, Molecular neurobiology of addiction, Am. J. Addict., 10, 201, 10.1080/105504901750532094 Zlebnik, 2014, Chronic wheel running affects cocaine-induced c-Fos expression in brain reward areas in rats, Behav. Brain Res., 261, 71, 10.1016/j.bbr.2013.12.012 Giustino, 2015, The role of the medial prefrontal cortex in the conditioning and extinction of fear, Front. Behav. Neurosci., 9, 10.3389/fnbeh.2015.00298 Sierra-Mercado, 2011, Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear, Neuropsychopharmacology, 36, 529, 10.1038/npp.2010.184 Whitaker, 2017, Bidirectional modulation of intrinsic excitability in rat prelimbic cortex neuronal ensembles and non-ensembles after operant learning, J. Neurosci., 37, 8845, 10.1523/JNEUROSCI.3761-16.2017 de Guglielmo, 2016, Recruitment of a neuronal ensemble in the central nucleus of the amygdala is required for alcohol dependence, J. Neurosci., 36, 9446, 10.1523/JNEUROSCI.1395-16.2016 Cole, 2020, Medial prefrontal cortex neural plasticity, orexin receptor 1 signaling, and connectivity with the lateral hypothalamus are necessary in cue-potentiated feeding, J. Neurosci., 40, 1744, 10.1523/JNEUROSCI.1803-19.2020 Warren, 2019, Separate vmPFC ensembles control cocaine self-administration versus extinction in rats, J. Neurosci., 39, 7394, 10.1523/JNEUROSCI.0918-19.2019 Liu, 2007, Imaging cerebral gene transcripts in live animals, J. Neurosci., 27, 713, 10.1523/JNEUROSCI.4660-06.2007 Cai, 2012, Multi-scale molecular photoacoustic tomography of gene expression, PLoS One, 7, 10.1371/journal.pone.0043999 Ozbay, 2018, Three dimensional two-photon brain imaging in freely moving mice using a miniature fiber coupled microscope with active axial-scanning, Sci. Rep., 8, 8108, 10.1038/s41598-018-26326-3 Yao, 2013, Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo, NeuroImage, 64, 257, 10.1016/j.neuroimage.2012.08.054 Hu, 2010, Neurovascular photoacoustic tomography, Front. Neuroenergetics, 2 Kasof, 1995, Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats, J. Neurosci., 15, 4238, 10.1523/JNEUROSCI.15-06-04238.1995 Xue, 2017, Selective inhibition of amygdala neuronal ensembles encoding nicotine-associated memories inhibits nicotine preference and relapse, Biol. Psychiatry, 82, 781, 10.1016/j.biopsych.2017.04.017 Manwar, 2020, Deep learning protocol for improved photoacoustic brain imaging, J. Biophotonics, 13, 10.1002/jbio.202000212 Mohammadi, 2020, Skull acoustic aberration correction in photoacoustic microscopy using a vector space similarity model: a proof-of-concept simulation study, Biomed. Opt. Express, 11, 5542, 10.1364/BOE.402027 Kamran Avanaki, 2019 James, 2021, Photoacoustic imaging of fear conditioning neuronal ensembles using a Fos-LacZ gene reporter system in the rat brain in vivo after intrathecal X-gal injection, Proc. SPIE Morgan, 1987, Mapping patterns of c-fos expression in the central nervous system after seizure, Science, 237, 192, 10.1126/science.3037702