A systematic review of the effects of transcranial photobiomodulation on brain activity in humans.
EEG
NIRS
fMRI
functional connectivity
human brain
low level light therapy
Journal
Reviews in the neurosciences
ISSN: 2191-0200
Titre abrégé: Rev Neurosci
Pays: Germany
ID NLM: 8711016
Informations de publication
Date de publication:
28 08 2023
28 08 2023
Historique:
received:
11
01
2023
accepted:
26
02
2023
medline:
4
8
2023
pubmed:
18
3
2023
entrez:
17
3
2023
Statut:
epublish
Résumé
In recent years, transcranial photobiomodulation (tPBM) has been developing as a promising method to protect and repair brain tissues against damages. The aim of our systematic review is to examine the results available in the literature concerning the efficacy of tPBM in changing brain activity in humans, either in healthy individuals, or in patients with neurological diseases. Four databases were screened for references containing terms encompassing photobiomodulation, brain activity, brain imaging, and human. We also analysed the quality of the included studies using validated tools. Results in healthy subjects showed that even after a single session, tPBM can be effective in influencing brain activity. In particular, the different transcranial approaches - using a focal stimulation or helmet for global brain stimulation - seemed to act at both the vascular level by increasing regional cerebral blood flow (rCBF) and at the neural level by changing the activity of the neurons. In addition, studies also showed that even a focal stimulation was sufficient to induce a global change in functional connectivity across brain networks. Results in patients with neurological disease were sparser; nevertheless, they indicated that tPBM could improve rCBF and functional connectivity in several regions. Our systematic review also highlighted the heterogeneity in the methods and results generated, together with the need for more randomised controlled trials in patients with neurological diseases. In summary, tPBM could be a promising method to act on brain function, but more consistency is needed in order appreciate fully the underlying mechanisms and the precise outcomes.
Identifiants
pubmed: 36927734
pii: revneuro-2023-0003
doi: 10.1515/revneuro-2023-0003
doi:
Types de publication
Systematic Review
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
671-693Informations de copyright
© 2023 Walter de Gruyter GmbH, Berlin/Boston.
Références
Altimus, C.M., Güler, A.D., Villa, K.L., McNeill, D.S., LeGates, T.A., and Hattar, S. (2008). Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc. Natl. Acad. Sci. U.S.A. 105: 19998–20003, https://doi.org/10.1073/pnas.0808312105 .
doi: 10.1073/pnas.0808312105
Attal, N., Poindessous-Jazat, F., De Chauvigny, E., Quesada, C., Mhalla, A., Ayache, S.S., Fermanian, C., Nizard, J., Peyron, R., Lefaucheur, J.P., et al.. (2021). Repetitive transcranial magnetic stimulation for neuropathic pain: a randomized multicentre sham-controlled trial. Brain 144: 3328–3339, https://doi.org/10.1093/brain/awab208 .
doi: 10.1093/brain/awab208
Babiloni, C., Binetti, G., Cassetta, E., Cerboneschi, D., Dal Forno, G., Del Percio, C., Ferreri, F., Ferri, R., Lanuzza, B., Miniussi, C., et al.. (2004). Mapping distributed sources of cortical rhythms in mild Alzheimer’s disease. a multicentric EEG study. Neuroimage 22: 57–67, https://doi.org/10.1016/j.neuroimage.2003.09.028 .
doi: 10.1016/j.neuroimage.2003.09.028
Babiloni, C., Del Percio, C., Caroli, A., Salvatore, E., Nicolai, E., Marzano, N., Lizio, R., Cavedo, E., Landau, S., Chen, K., et al.. (2016). Cortical sources of resting state EEG rhythms are related to brain hypometabolism in subjects with Alzheimer’s disease: an EEG-PET study. Neurobiol. Aging 48: 122–134, https://doi.org/10.1016/j.neurobiolaging.2016.08.021 .
doi: 10.1016/j.neurobiolaging.2016.08.021
Barrett, D.W. and Gonzalez-Lima, F. (2013). Transcranial infrared laser stimulation produces beneficial cognitive and emotional effects in humans. Neuroscience 230: 13–23, https://doi.org/10.1016/j.neuroscience.2012.11.016 .
doi: 10.1016/j.neuroscience.2012.11.016
Blanco, N.J., Saucedo, C.L., and Gonzalez-Lima, F. (2017a). Transcranial infrared laser stimulation improves rule-based, but not information-integration, category learning in humans. Neurobiol. Learn. Mem. 7, https://doi.org/10.1016/j.nlm.2016.12.016 .
doi: 10.1016/j.nlm.2016.12.016
Blanco, N.J., Maddox, W.T., and Gonzalez-Lima, F. (2017b). Improving executive function using transcranial infrared laser stimulation. J. Neuropsychol. 11: 14–25, https://doi.org/10.1111/jnp.12074 .
doi: 10.1111/jnp.12074
Blivet, G., Meunier, J., Roman, F.J., and Touchon, J. (2018). Neuroprotective effect of a new photobiomodulation technique against Aβ25–35 peptide-induced toxicity in mice: novel hypothesis for therapeutic approach of Alzheimer’s disease suggested. Alzheimer’s Dementia 4: 54–63, https://doi.org/10.1016/j.trci.2017.12.003 .
doi: 10.1016/j.trci.2017.12.003
Blivet, G., Relano-Gines, A., Wachtel, M., and Touchon, J. (2022). A randomized, double-blind, and sham-controlled trial of an innovative brain-gut photobiomodulation therapy: safety and patient compliance. J. Alzheim. Dis. 90: 811–822, https://doi.org/10.3233/jad-220467 .
doi: 10.3233/jad-220467
Cardoso, F., dos, S., de Souza Oliveira Tavares, C., Araujo, B.H.S., Mansur, F., Lopes-Martins, R.Á.B., and Gomes da Silva, S. (2022). Improved spatial memory and neuroinflammatory profile changes in aged rats submitted to photobiomodulation therapy. Cell. Mol. Neurobiol. 42: 1875–1886, https://doi.org/10.1007/s10571-021-01069-4 .
doi: 10.1007/s10571-021-01069-4
Cardoso, F., dos, S., Martins, R.Á.B.L., and Gomes da Silva, S. (2020). Therapeutic potential of photobiomodulation in Alzheimer’s disease: a systematic review. J Lasers Med. 11: S16–S22, https://doi.org/10.34172/jlms.2020.s3 .
doi: 10.34172/jlms.2020.s3
Cassano, P., Tran, A.P., Katnani, H., Bleier, B.S., Hamblin, M.R., Yuan, Y., and Fang, Q. (2019). Selective photobiomodulation for emotion regulation: model-based dosimetry study. Neurophotonics 6: 1, https://doi.org/10.1117/1.nph.6.1.015004 .
doi: 10.1117/1.nph.6.1.015004
Chaieb, L., Antal, A., Masurat, F., and Paulus, W. (2015). Neuroplastic effects of transcranial near-infrared stimulation (tNIRS) on the motor cortex. Front. Behav. Neurosci. 9: 147, https://doi.org/10.3389/fnbeh.2015.00147 .
doi: 10.3389/fnbeh.2015.00147
Chan, A.S., Lee, T.L., Hamblin, M.R., and Cheung, M.C. (2021). Photobiomodulation enhances memory processing in older adults with mild cognitive impairment: a functional near-infrared spectroscopy study. J. Alzheim. Dis. 83: 1471–1480, https://doi.org/10.3233/jad-201600 .
doi: 10.3233/jad-201600
Chan, A.S., Lee, T.L., Yeung, M.K., and Hamblin, M.R. (2019). Photobiomodulation improves the frontal cognitive function of older adults. Int. J. Geriatr. Psychiatr. 34: 369–377, https://doi.org/10.1002/gps.5039 .
doi: 10.1002/gps.5039
Chao, L. (2019). Effects of home photobiomodulation treatments on cognitive and behavioural function, cerebral perfusion, and resting-state functional connectivity in patients with dementia: a pilot trial. Photobiomodul Photomed Laser Surg 37: 133–141, https://doi.org/10.1089/photob.2018.4555 .
doi: 10.1089/photob.2018.4555
Chao, L., Barlow, C., Karimpoor, M., and Lim, L. (2020). Changes in brain function and structure after self-administered home photobiomodulation treatment in a concussion case. Front. Neurol. 11: 952, https://doi.org/10.3389/fneur.2020.00952 .
doi: 10.3389/fneur.2020.00952
Chen, A.C.H., Arany, P.R., Huang, Y.Y., Tomkinson, E.M., Sharma, S.K., Kharkwal, G.B., Saleem, T., Mooney, D., Yull, F.E., Blackwell, T.S., et al.. (2011). Low-level laser therapy activates NF-κB via generation of reactive oxygen species in mouse embryonic fibroblasts. PLoS One 6: e22453, https://doi.org/10.1371/journal.pone.0022453 .
doi: 10.1371/journal.pone.0022453
Claus, J.J., De Visser, B.W.O., Bour, L.J., Walstra, G.J., Hijdra, A., Verbeeter, B.Jr, Van Royen, E.A., Kwa, V.I., and van Gool, W.A. (2000). Determinants of quantitative spectral electroencephalography in early Alzheimer’s disease: cognitive function, regional cerebral blood flow, and computed tomography. Dement. Geriatr. Cognit. Disord. 11: 81–89, https://doi.org/10.1159/000017219 .
doi: 10.1159/000017219
Darlot, F., Moro, C., El Massri, N., Chabrol, C., Johnstone, D.M., Reinhart, F., Agay, D., Torres, N., Bekha, D., Auboiroux, V., et al.. (2016). Near-infrared light is neuroprotective in a monkey model of Parkinson disease: neuroprotection after NIr. Ann. Neurol. 79: 59–75, https://doi.org/10.1002/ana.24542 .
doi: 10.1002/ana.24542
De Freitas, L. and Hamblin, M.R. (2016). Proposed mechanisms of photobiomodulation or low level light therapy. IEEE J. Sel. Top. Quant. Electron. 22: 7000417, https://doi.org/10.1109/jstqe.2016.2561201 .
doi: 10.1109/jstqe.2016.2561201
Dmochowski, G.M., Shereen, A.D., Berisha, D., and Dmochowski, J.P. (2020). Near-infrared light increases functional connectivity with a non-thermal mechanism. Cereb Cortex Commun. 1: 1–12, https://doi.org/10.1093/texcom/tgaa004 .
doi: 10.1093/texcom/tgaa004
El Khoury, H., Mitrofanis, J., and Henderson, L.A. (2019). Exploring the effects of near infrared light on resting and evoked brain activity in humans using magnetic resonance imaging. Neurosciences 422: 161–171, https://doi.org/10.1016/j.neuroscience.2019.10.037 .
doi: 10.1016/j.neuroscience.2019.10.037
El Khoury, H., Mitrofanis, J., and Henderson, L.A. (2021). Does photobiomodulation influence the resting-state networks in young human subjects? Exp. Brain Res. 239: 435–449, https://doi.org/10.1007/s00221-020-05981-x .
doi: 10.1007/s00221-020-05981-x
Figueiro-Longo, M.G., Tan, C.O., Chan, S., Welt, J., Avesta, A., Ratai, E., Mercaldo, N.D., Yendiki, A., Namati, J., Chico-Calero, I., et al.. (2020). Effect of transcranial low-level light therapy vs sham therapy among patients with moderate traumatic brain injury. JAMA Netw. Open 3: e2017337, https://doi.org/10.1001/jamanetworkopen.2020.17337 .
doi: 10.1001/jamanetworkopen.2020.17337
Gerace, E., Cialdai, F., Sereni, E., Lana, D., Nosi, D., Giovannini, M.G., Monici, M., and Mannaioni, G. (2021). NIR laser photobiomodulation induces neuroprotection in an in vitro model of cerebral hypoxia/ischemia. Mol. Neurobiol. 58: 5383–5395, https://doi.org/10.1007/s12035-021-02496-6 .
doi: 10.1007/s12035-021-02496-6
Ghaderi, A.H., Jahan, A., Akrami, F., and Salimi, M.M. (2021). Transcranial photobiomodulation changes topology, synchronizability, and complexity of resting state brain networks. J. Neural. Eng. 18: 046048, https://doi.org/10.1088/1741-2552/abf97c .
doi: 10.1088/1741-2552/abf97c
Gutiérrez-Menéndez, A., Martínez, J.A., Méndez, M., and Arias, J.L. (2022). No effects of photobiomodulation on prefrontal cortex and hippocampal cytochrome c oxidase activity and expression of c-Fos protein of young male and female rats. Front. Neurosci. 16: 897225, https://doi.org/10.3389/fnins.2022.897225 .
doi: 10.3389/fnins.2022.897225
Hacke, W., Schellinger, P.D., Albers, G.W., Bornstein, N.M., Dahlof, B.L., Kasner, S.E., Shuaib, A., Richieri, S.P., Dilly, S.G., Zivin, J., et al.. (2014). Transcranial laser therapy in acute stroke treatment: results of neurothera effectiveness and safety trial 3, a phase III clinical en point device trial. Stroke 45: 3187–3193, https://doi.org/10.1161/strokeaha.114.005795 .
doi: 10.1161/strokeaha.114.005795
Hamblin, M.R. (2016). Shining light on the head: photobiomodulation for brain disorders. BBA Clin. 6: 113–124, https://doi.org/10.1016/j.bbacli.2016.09.002 .
doi: 10.1016/j.bbacli.2016.09.002
Hamblin, M.R. (2017). Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys. 4: 337–361, https://doi.org/10.3934/biophy.2017.3.337 .
doi: 10.3934/biophy.2017.3.337
Hamblin, M.R. and Liebert, A. (2022). Photobiomodulation therapy mechanisms beyond cytochrome c oxidase. Photobiomodul. Photomed. Laser Surg. 40: 75–77, https://doi.org/10.1089/photob.2021.0119 .
doi: 10.1089/photob.2021.0119
Hamilton, C.L., El Khoury, H., Hamilton, D., Nicklason, F., and Mitrofanis, J. (2019). “Buckets”: early observations on the use of red and infrared light helmets in Parkinson’s disease patients. Photobiomodul. Photomed. Laser Surg. 37: 615–622, https://doi.org/10.1089/photob.2019.4663 .
doi: 10.1089/photob.2019.4663
Haroon, J., Mahdavi, K., Zielinski, M.A., Habelhah, B., Chan, L., Bystritsky, A., Beoerra, S. and Jordan, S. (2021). A case of COVID-encephalopathy imaged with fMRI and treated with near infrared light. Brain Stimul. 14:1444–1446, https://doi.org/10.1016/j.brs.2021.10.377 .
doi: 10.1016/j.brs.2021.10.377
Hipskind, S.G., Grover, F.L., Fort, T.R., Helffenstein, D., Burke, T.J., Quint, S.A., Bussiere, G., Stone, M., and Hurtado, T. (2019). Pulsed transcranial red/near-infrared light therapy using light-emitting diodes improves cerebral blood flow and cognitive function in veterans with chronic traumatic brain injury: a case series. Photobiomodul. Photomed. Laser Surg. 37: 77–84, https://doi.org/10.1089/photob.2018.4489 .
doi: 10.1089/photob.2018.4489
Holmes, E., Barrett, D.W., Saucedo, C.L., O’Connor, P., Liu, H., and Gonzalez-Lima, F. (2019). Cognitive enhancement by transcranial photobiomodulation is associated with cerebrovascular oxygenation of the prefrontal cortex. Front. Neurosci. 13: 1129, https://doi.org/10.3389/fnins.2019.01129 .
doi: 10.3389/fnins.2019.01129
Huisa, B.N., Stemer, A.B., Walker, M.G., Rapp, K., Meyer, B.C., and Zivin, J.A. (2013). Transcranial laser therapy for acute ischemic stroke: a pooled analysis of NEST-1 and NEST-2. Int. J. Stroke 8: 315–320, https://doi.org/10.1111/j.1747-4949.2011.00754.x .
doi: 10.1111/j.1747-4949.2011.00754.x
Jafari, Z., Kolb, B.E., and Mohajerani, M.H. (2020). Neural oscillations and brain stimulation in Alzheimer’s disease. Prog. Neurobiol. 194: 101878, https://doi.org/10.1016/j.pneurobio.2020.101878 .
doi: 10.1016/j.pneurobio.2020.101878
Jagdeo, J.R., Adams, L.E., Brody, N.I., and Siegel, D.M. (2012). Transcranial red and near infrared light transmission in a cadaveric model. PLoS One 7: e47460, https://doi.org/10.1371/journal.pone.0047460 .
doi: 10.1371/journal.pone.0047460
Jahan, A., Nazari, M.A., Mahmoudi, J., Salehpour, F., and Moghadam Salimi, M. (2019). Transcranial near-infrared photobiomodulation could modulate brain electrophysiological features and attentional performances in healthy young adults. Laser Med. Sci. 34: 1193–1200, https://doi.org/10.1007/s10103-018-02710-3 .
doi: 10.1007/s10103-018-02710-3
Jann, K., Kottlow, M., Dierks, T., Boesch, C., and Koenig, T. (2010). Topographic electrophysiological signatures of fMRI resting state networks. PLoS One 5: e12945, https://doi.org/10.1371/journal.pone.0012945 .
doi: 10.1371/journal.pone.0012945
Johnstone, D.M., el Massri, N., Moro, C., Spana, S., Wang, X.S., Torres, N., Chabrol, C., De Jaeger, X., Reinhart, F., Purushothuman, S., et al.. (2014). Indirect application of near infrared light induces neuroprotection in a mouse model of parkinsonism – an abscopal neuroprotective effect. Neuroscience 274: 93–101, https://doi.org/10.1016/j.neuroscience.2014.05.023 .
doi: 10.1016/j.neuroscience.2014.05.023
Karu, T. (2010). Mitochondrial mechanisms of photobiomodulation in context of new data about multiple roles of ATP. Photomed Laser Surg. 28: 159–160, https://doi.org/10.1089/pho.2010.2789 .
doi: 10.1089/pho.2010.2789
Knyazev, G.G. (2011). EEG delta oscillations as a correlate of basic homeostatic and motivational processes. Neurosci. Biobehav. Rev. 36: 677–695, https://doi.org/10.1016/j.neubiorev.2011.10.002 .
doi: 10.1016/j.neubiorev.2011.10.002
Konstantinović, L.M., Jelić, M.B., Jeremić, A., Stevanović, V.B., Milanović, S.D., and Filipović, S.R. (2013). Transcranial application of near-infrared low-level laser can modulate cortical excitability. Laser Surg. Med. 45: 648–653, https://doi.org/10.1002/lsm.22190 .
doi: 10.1002/lsm.22190
Korotkova, T., Ponomarenko, A., Monaghan, C.K., Poulter, S.L., Cacucci, F., Wills, T., Hasselmo, M.E., and Lever, C. (2018). Reconciling the different faces of hippocampal theta: the role of theta oscillations in cognitive, emotional and innate behaviors. Neurosci. Biobehav. Rev. 85: 65–80, https://doi.org/10.1016/j.neubiorev.2017.09.004 .
doi: 10.1016/j.neubiorev.2017.09.004
Kringelbach, M.L., Jenkinson, N., Owen, S.L.F., and Aziz, T.Z. (2007). Translational principles of deep brain stimulation. Nat. Rev. Neurosci. 8: 623–635, https://doi.org/10.1038/nrn2196 .
doi: 10.1038/nrn2196
Lample, Y., Zivin, J.A., Fisher, M., Lew, R., Welin, L., Dahlof, B., Borenstein, P., Andersson, B., Perez, J., Caparo, C., et al.. (2007). Infrared Laser Therapy for ischemic stroke: a new treatment strategy. Stroke 38: 1843–1849, https://doi.org/10.1161/strokeaha.106.478230 .
doi: 10.1161/strokeaha.106.478230
Lapchak, P.A., Boitano, P.D., Butte, P.V., Fisher, D.J., Hölscher, T., Ley, E.J., Nuño, M., Voie, A.H., and Rajput, P.S. (2015). Transcranial near-infrared laser transmission (NILT) profiles (800 nm): systematic comparison in four common research species. PLoS One 10: e0127580, https://doi.org/10.1371/journal.pone.0127580 .
doi: 10.1371/journal.pone.0127580
Li, T., Xue, C., Wang, P., Li, Y., and Wu, L. (2017). Photon penetration depth in human brain for light stimulation and treatment: a realistic monte carlo simulation study. J. Innov. Opt. Health Sci. 10: 1743002, https://doi.org/10.1142/s1793545817430027 .
doi: 10.1142/s1793545817430027
Liebert, A., Bicknell, B., Laakso, A., Heller, G., Jalilitabaei, P., Tilley, S., Mitrofanis, J., and Kiat, H. (2021). Improvements in clinical signs of Parkinson’s disease using photobiomodulation: a prospective proof-of-concept study. BMC Neurol. 21: 256, https://doi.org/10.1186/s12883-021-02248-y .
doi: 10.1186/s12883-021-02248-y
Lockley, S.W., Evans, E.E., Scheer, F.A.J.L., Brainard, G.C., Czeisler, C.A., and Aeschbach, D. (2006). Short-wavelength sensitivity for the direct effects of light on alertness, vigilance, and the waking electroencephalogram in humans. Sleep 29: 161–168.
Ma, L.L., Wang, Y.Y., Yang, Z.H., Huang, D., Weng, H., and Zeng, X.T. (2020). Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better? Mil Med Res 7: 7, https://doi.org/10.1186/s40779-020-00238-8 .
doi: 10.1186/s40779-020-00238-8
Maiello, M., Losiewicz, O.M., Bui, E., Spera, V., Hamblin, M.R., Marques, L., and Cassano, P. (2019). Transcranial photobiomodulation with near-infrared light for generalized anxiety disorder: a pilot study. Photobiomodul. Photomed. Laser Surg. 37: 644–650, https://doi.org/10.1089/photob.2019.4677 .
doi: 10.1089/photob.2019.4677
Mantini, D., Perrucci, M.G., Del Gratta, C., Romani, G.L., and Corbetta, M. (2007). Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. USA 104: 13170–13175, https://doi.org/10.1073/pnas.0700668104 .
doi: 10.1073/pnas.0700668104
Marashian, S.M., Hashemian, M., Pourabdollah, M., Nasseri, M., Mahmoudian, S., Reinhart, F., and Eslaminejad, A. (2022). Photobiomodulation improves serum cytokine response in mild to moderate COVID-19: the first randomized, double-blind, placebo controlled, pilot study. Front. Immunol. 13: 929837, https://doi.org/10.3389/fimmu.2022.929837 .
doi: 10.3389/fimmu.2022.929837
Mitrofanis, J. (2019). The light is photobiomodulation. In: Hamblin, M.R. (Ed.). Run in the light: exploring exercise and photobiomodulation in Parkinson’s disease . IOP Publishing in Photomedicine and Biophotonics, Bristol, UK.
Mohan, A., Roberto, A.J., Mohan, A., Lorenzo, A., Jones, K., Carney, M.J., Liogier-Weyback, L., Hwang, S., and Lapidus, K.A.B. (2016). The significance of the default mode network (DMN) in neurological and neuropsychiatric disorders: a review. Yale J. Biol. Med. 89: 49–57.
Moisset, X., de Andrade, D.C., and Bouhassira, D. (2015). From pulses to pain relief: an update on the mechanisms of rTMS-induced analgesic effects. Eur. J. Pain 20: 689–700, https://doi.org/10.1002/ejp.811 .
doi: 10.1002/ejp.811
Moola, S., Munn, Z., Tufanaru, C., Aromataris, E., Sears, K., Sfetcu, R., Curri, M., Lisy, K., Qureshi, R., Mattis, P., et al.. (2020). Chapter 7: systematic reviews of etiology and risk. In: Aromataris, E. and Munn, Z. (Eds.), JBI manual for evidence synthesis . JBI.
Moro, C., Massri, N.E., Torres, N., Ratel, D., De Jaeger, X., Chabrol, C., Perraut, F., Bourgerette, A., Berger, M., Purushothuman, S., et al.. (2014). Photobiomodulation inside the brain: a novel method of applying near-infrared light intracranially and its impact on dopaminergic cell survival in MPTP-treated mice. J. Neurosurg. 120: 670–683, https://doi.org/10.3171/2013.9.jns13423 .
doi: 10.3171/2013.9.jns13423
Naeser, M.A., Zafonte, R., Krengel, M.H., Martin, P.I., Frazier, J., Hamblin, M.R., Knight, J.A., Meehan, W.P.III, and Baker, E. (2014). Significant improvements in cognitive performance post-transcranial, red/near-infrared light-emitting diode treatments in chronic, mild traumatic brain injury: open-protocol study. J. Neurotrauma 31: 1008–1017, https://doi.org/10.1089/neu.2013.3244 .
doi: 10.1089/neu.2013.3244
Nguyen, G. and Postnova, S. (2021). Progress in modelling of brain dynamics during anaesthesia and the role of sleep-wake circuitry. Biochem. Pharmacol. 191: 114388, https://doi.org/10.1016/j.bcp.2020.114388 .
doi: 10.1016/j.bcp.2020.114388
Nizamutdinov, D., Qi, X., Berman, M.H., Dougal, G., Dayawansa, S., Wu, E., Yi, S.S., Stevens, A.B., and Huang, J.H. (2021). Transcranial near infrared light stimulations improve cognition in patients with dementia. Aging Dis 12: 954–963, https://doi.org/10.14336/ad.2021.0229 .
doi: 10.14336/ad.2021.0229
PRISMA-P Group , Moher, D., Shamseer, L., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P. and Stewart, L.A. (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P). Syst. Rev. 4: 1, https://doi.org/10.1186/2046-4053-4-1 .
doi: 10.1186/2046-4053-4-1
Pruitt, T., Wang, X., Wu, A., Kallioniemi, E., Husain, M.M., and Liu, H. (2020). Transcranial photobiomodulation (tPBM) with 1,064-nm laser to improve cerebral metabolism of the human brain in vivo. Laser Surg. Med. 52: 807–813, https://doi.org/10.1002/lsm.23232 .
doi: 10.1002/lsm.23232
Purushothuman, S., Johnstone, D.M., Nandasena, C., Mitrofanis, J., and Stone, J. (2014). Photobiomodulation with near infrared light mitigates Alzheimer’s disease-related pathology in cerebral cortex – evidence from two transgenic mouse models. Alzheimer’s Res. Ther. 6: 2, https://doi.org/10.1186/alzrt232 .
doi: 10.1186/alzrt232
Rupel, K., Zupin, L., Colliva, A., Kamada, A., Poropat, A., Ottaviani, G., Gobbo, M., Fanfoni, L., Gratton, R., Santoro, M., et al.. (2018). Photobiomodulation at multiple wavelengths differentially modulates oxidative stress in vitro and in vivo. Oxid. Med. Cell. Longev. 2018: 1–11, https://doi.org/10.1155/2018/6510159 .
doi: 10.1155/2018/6510159
Salehpour, F., Ahmadian, N., Rasta, S.H., Farhoudi, M., Karimi, P., and Sadigh-Eteghad, S. (2017). Transcranial low-level laser therapy improves brain mitochondrial function and cognitive impairment in D-galactose–induced aging mice. Neurobiol. Aging 58: 140–150, https://doi.org/10.1016/j.neurobiolaging.2017.06.025 .
doi: 10.1016/j.neurobiolaging.2017.06.025
Salehpour, F., De Taboada, L., Cassano, P., Kamari, F., Mahmoudi, J., Ahmadi-Kandjani, S., Rasta, S.H., and Sadigh-Eteghad, S. (2018). A protocol for transcranial photobiomodulation therapy in mice. JoVE 18: 59076, https://doi.org/10.3791/59076-v .
doi: 10.3791/59076-v
Salehpour, F., Majdi, A., Pazhuhi, M., Ghasemi, F., Khademi, M., Pashazadeh, F., Hamblin, M.R., and Cassano, P. (2019). Transcranial photobiomodulation improves cognitive performance in young healthy adults: a systematic review and meta-analysis. Photobiomodul. Photomed. Laser Surg. 37: 635–643, https://doi.org/10.1089/photob.2019.4673 .
doi: 10.1089/photob.2019.4673
Salgado, A.S.I., Zângaro, R.A., Parreira, R.B., and Kerppers, I.I. (2015). The effects of transcranial LED therapy (TCLT) on cerebral blood flow in the elderly women. Laser Med. Sci. 30: 339–346, https://doi.org/10.1007/s10103-014-1669-2 .
doi: 10.1007/s10103-014-1669-2
Saucedo, C.L., Courtois, E.C., Wade, Z.S., Kelley, M.N., Kheradbin, N., Barrett, D.W., and Gonzalez-Lima, F. (2021). Transcranial laser stimulation: mitochondrial and cerebrovascular effects in younger and older healthy adults. Brain Stimul. 14: 440–449, https://doi.org/10.1016/j.brs.2021.02.011 .
doi: 10.1016/j.brs.2021.02.011
Schiffer, F., Johnston, A.L., Ravichandran, C., Polcari, A., Teicher, M.H., Webb, R.H. and Hamblin, M.R. (2009). Psychological benefits 2 and 4 weeks after a single treatment with near infrared light to the forehead: a pilot study of 10 patients with major depression and anxiety. Behav. Brain Funct. 5: 46, https://doi.org/10.1186/1744-9081-5-46 .
doi: 10.1186/1744-9081-5-46
Shahdadian, S., Wang, X., Wanniarachchi, H., Chaudhari, A., Truong, N.C.G., and Liu, H. (2022). Neuromodulation of brain power topography and network topology by prefrontal transcranial photobiomodulation. J. Neural. Eng. 19: 10.1088, https://doi.org/10.1088/1741-2552/ac9ede .
doi: 10.1088/1741-2552/ac9ede
Shamseer, L., Moher, D., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P., and Stewart, L.A., and the PRISMA-P Group . (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. Br. Med. J. 349: g7647, https://doi.org/10.1136/bmj.g7647 .
doi: 10.1136/bmj.g7647
Sharma, S.K., Kharkwal, G.B., Sajo, M., Huang, Y.Y., De Taboada, L., McCarthy, T., and Hamblin, M.R. (2011). Dose response effects of 810 nm laser light on mouse primary cortical neurons. Laser Surg. Med. 43: 851–859, https://doi.org/10.1002/lsm.21100 .
doi: 10.1002/lsm.21100
Shaw, V., Spana, S., Ashkan, K., Benabid, A.L., Stone, J., Baker, G.E., and Mitrofanis, J. (2010). Neuroprotection of midbrain dopaminergic cells in MPTP-treated mice after near-infrared light treatment. J. Comp. Neurol. 518: 25–40, https://doi.org/10.1002/cne.22207 .
doi: 10.1002/cne.22207
Shinhmar, H., Grewal, M., Sivaprasad, S., Hogg, C., Chong, V., Neveu, M., and Jeffery, G. (2020). Optically improved mitochondrial function redeems aged human visual decline. J. Gerontol. A. Biol. Sci. Med. Sci. 75: e49–e52, https://doi.org/10.1093/gerona/glaa155 .
doi: 10.1093/gerona/glaa155
Sommer, A.P., Haddad, M.Kh., and Fecht, H.J. (2015). Light effect on water viscosity: implication for ATP biosynthesis. Sci. Rep. 5: 12029, https://doi.org/10.1038/srep12029 .
doi: 10.1038/srep12029
Song, P., Han, T., Lin, H., Li, S., Huang, Q., Dai, X., Wang, R., and Wang, Y. (2020). Transcranial near-infrared stimulation may increase cortical excitability recorded in humans. Brain Res. Bull. 155: 155–158, https://doi.org/10.1016/j.brainresbull.2019.12.007 .
doi: 10.1016/j.brainresbull.2019.12.007
Spera, V., Sitnikova, T., Ward, M.J., Farzam, P., Hughes, J., Gazecki, S., Bui, E., Maiello, M., De Taboada, L.D., Hamblin, M.R., et al.. (2021). Pilot study on dose-dependent effects of transcranial photobiomodulation on brain electrical oscillations: a potential therapeutic target in Alzheimer’s disease. J. Alzheim. Dis. 83: 1481–1498, https://doi.org/10.3233/jad-210058 .
doi: 10.3233/jad-210058
Sterne, J.A.C., Savovic, J., Page, M.J., Elbers, R.G., Blencowe, N.S., Boutron, I., Cates, C.J., Cheng, H.Y., Corbett, M.S., Eldridge, S.M., et al.. (2019). RoB2: a revised tool for assessing risk of bias in randomised trials. Br. Med. J. 366: I4898, https://doi.org/10.1136/bmj.l4898 .
doi: 10.1136/bmj.l4898
Tedford, C.E., DeLapp, S., Jacques, S., and Anders, J. (2015). Quantitative analysis of transcranial and intraparenchymal light penetration in human cadaver brain tissue. Laser Surg. Med. 47: 312–322, https://doi.org/10.1002/lsm.22343 .
doi: 10.1002/lsm.22343
Tian, F., Hase, S.N., Gonzalez-Lima, F., and Liu, H. (2016). Transcranial laser stimulation improves human cerebral oxygenation. Laser Surg. Med. 48: 343–349, https://doi.org/10.1002/lsm.22471 .
doi: 10.1002/lsm.22471
Uozumi, Y., Nawashiro, H., Sato, S., Kawauchi, S., Shima, K., and Kikuchi, M. (2010). Targeted increase in cerebral blood flow by transcranial near-infrared laser irradiation: increased CBF by near infrared laser irradiation. Laser Surg. Med. 42: 566–576, https://doi.org/10.1002/lsm.20938 .
doi: 10.1002/lsm.20938
Urquhart, E.L., Wanniarachchi, H., Wang, X., Gonzalez-Lima, F., Alexandrakis, G. and Liu, H. (2020). Transcranial photobiomodulation-induced changes in human brain functional connectivity and network metrics mapped by whole-head functional near-infrared spectroscopy in vivo. Biomed Opt. Express. 11: 5783–5799, https://doi.org/10.1364/boe.402047 .
doi: 10.1364/boe.402047
Vanderwalle, G., Maquet, P., and Dijk, D.J. (2009). Light as a modulator of cognitive brain function. Trends Cognit Neurosci 13: 429–438, https://doi.org/10.1016/j.tics.2009.07.004 .
doi: 10.1016/j.tics.2009.07.004
Vatner, S.F., Zhang, J., Oydanich, M., Berkman, T., Naftalovich, R., and Vatner, D.E. (2020). Healthful aging mediated by inhibition of oxidative stress. Ageing Res. Rev. 64: 101194, https://doi.org/10.1016/j.arr.2020.101194 .
doi: 10.1016/j.arr.2020.101194
Wang, X., Dmochowski, J.P., Zeng, L., Kallioniemi, E., Husain, M., Gonzalez-Lima, F., and Liu, H. (2019). Transcranial photobiomodulation with 1064-nm laser modulates brain electroencephalogram rhythms. Neurophotonics 6: 1, https://doi.org/10.1117/1.nph.6.2.025013 .
doi: 10.1117/1.nph.6.2.025013
Wang, X., Ma, L.C., Shahdadian, S., Wu, A., Truong, N.C.D., and Liu, H. (2022a). Metabolic connectivity and hemodynamic-metabolic coherence of human prefrontal cortex at rest and post photobiomodulation assessed by dual-channel broadband NIRS. Metabolites 12: 42, https://doi.org/10.3390/metabo12010042 .
doi: 10.3390/metabo12010042
Wang, X., Tian, F., Reddy, D.D., Nalawade, S.S., Barrett, D.W., Gonzalez-Lima, F., and Liu, H. (2017). Up-regulation of cerebral cytochrome-c-oxidase and hemodynamics by transcranial infrared laser stimulation: a broadband near-infrared spectroscopy study. J. Cerebr. Blood Flow Metabol. 37: 3789–3802, https://doi.org/10.1177/0271678x17691783 .
doi: 10.1177/0271678x17691783
Wang, X., Wanniarachchi, H., Wu, A., Gonzalez-Lima, F., and Liu, H. (2021). Transcranial photobiomodulation and thermal stimulation induce distinct topographies of EEG alpha and beta power changes in healthy humans. Sci. Rep. 11: 18917, https://doi.org/10.1038/s41598-021-97987-w .
doi: 10.1038/s41598-021-97987-w
Wang, X., Wanniarachchi, H., Wu, A., and Liu, H. (2022b). Combination of group singular value decomposition and eLORETA identifies human EEG networks and responses to transcranial photobiomodulation. Front. Hum. Neurosci. 16: 853909, https://doi.org/10.3389/fnhum.2022.853909 .
doi: 10.3389/fnhum.2022.853909
Wong-Riley, M.T.T., Ling Liang, H., Eells, J.T., Chance, B., Henry, M., Buchmann, E., Kane, M., and Whelan, H.T. (2005). Photobiomodulation directly benefits primary neurons functionally inactivated by toxins. J. Biol. Chem. 280: 4761–4771, https://doi.org/10.1074/jbc.m409650200 .
doi: 10.1074/jbc.m409650200
Wu, Q., Wang, X., Liu, H., and Zeng, L. (2020). Learning hemodynamic effect of transcranial infrared laser stimulation using longitudinal data analysis. IEEE J. Biomed. Health Inform. 24: 1772–1779, https://doi.org/10.1109/jbhi.2019.2951772 .
doi: 10.1109/jbhi.2019.2951772
Xie, K., El Khoury, H., Mitrofanis, J. and Austin, P.J. (2023). A systematic review of the effect of photobiomodulation on the neuroinflammatory response in animal models of neurodegenerative diseases. Rev. Neurosci. 34: 459–481. https://doi.org/10.1515/revneuro-2022-0109 .
doi: 10.1515/revneuro-2022-0109
Yao, L., Qian, Z., Liu, Y., Fang, Z., Li, W., and Xing, L. (2021). Effects of stimulating frequency of NIR LEDs light irradiation on forehead as quantified by EEG measurements. J. Innov. Opt. Health Sci. 14: 2050025, https://doi.org/10.1142/s179354582050025x .
doi: 10.1142/s179354582050025x
Yuan, Y., Cassano, P., Pias, M., and Fang, Q. (2020). Transcranial photobiomodulation with near-infrared light from childhood to elderliness: simulation of dosimetry. Neurophotonics 7: 015009-1-015009-15, https://doi.org/10.1117/1.nph.7.1.015009 .
doi: 10.1117/1.nph.7.1.015009
Zomorrodi, R., Loheswaran, G., Pushparaj, A., and Lim, L. (2019). Pulsed near infrared transcranial and intranasal photobiomodulation significantly modulates neural oscillations: a pilot exploratory study. Sci. Rep. 9: 6309, https://doi.org/10.1038/s41598-019-42693-x .
doi: 10.1038/s41598-019-42693-x