Metabolic Connectivity and Hemodynamic-Metabolic Coherence of Human Prefrontal Cortex at Rest and Post Photobiomodulation Assessed by Dual-Channel Broadband NIRS

Abstract

Billions of neurons in the human brain form neural networks with oscillation rhythms. Infra-slow oscillation (ISO) presents three main physiological sources: endogenic, neurogenic, and myogenic vasomotions. Having an in vivo methodology for the absolute quantification of ISO from the human brain can facilitate the detection of brain abnormalities in cerebral hemodynamic and metabolic activities. In this study, we introduced a novel measurement-plus-analysis framework for the non-invasive quantification of prefrontal ISO by (1) taking dual-channel broadband near infrared spectroscopy (bbNIRS) measurements from 12 healthy humans during a 6-min rest and 4-min post transcranial photobiomodulation (tPBM) and (2) performing wavelet transform coherence (WTC) analysis on the measured time series data. The WTC indexes (IC, between 0 and 1) enabled the assessment of ipsilateral hemodynamic-metabolic coherence and bilateral functional connectivity in each ISO band of the human prefrontal cortex. At rest, bilateral hemodynamic connectivity was consistent across the three ISO bands (IC ≅ 0.66), while bilateral metabolic connectivity was relatively weaker. For post-tPBM/sham comparison, our analyses revealed three key findings: 8-min, right-forehead, 1064-nm tPBM (1) enhanced the amplitude of metabolic oscillation bilaterally, (2) promoted the bilateral metabolic connectivity of neurogenic rhythm, and (3) made the main effect on endothelial cells, causing alteration of hemodynamic-metabolic coherence on each side of the prefrontal cortex.

Enhancement of Frequency-Specific Hemodynamic Power and Functional Connectivity by Transcranial Photobiomodulation in Healthy Humans

“…Moreover, the observation that tPBM enabled to strongly modulate myogenic oscillation within cerebral hemodynamic ISO across the human whole head is also highly consistent with our recent article (Wang et al, 2022). Accordingly, tPBM significantly enhanced the spectral amplitude of [HbO] in the myogenic bands by 23% near the tPBM site compared to the sham condition (Wang et al, 2022). Putting all the knowledge and recent findings together, our observations could be explained or interpreted as follows: tPBM started a cascade process by (1) first triggering the release of NO (besides photo-oxidation of CCO), (2) causing increases in endogenic oscillation and FC, (3) giving rise to the relaxation of the vascular smooth muscle, and thus (4) resulting in changes in myogenic oscillations as well as increases in myogenic FC.…”

“…Furthermore, the strong modulation ability of tPBM on endogenic oscillation within cerebral hemodynamic ISO across the human whole head seen in this study is highly consistent with and well supported by another just-published article of our group (Wang et al, 2022). The report was based on dual-channel, bbNIRS measurements taken from a completely different group of participants and performed by different operators.…”

“…Similar to the endogenic frequency band, the Post-Pre pair of the myogenic frequency band exhibited significant improvement in FC among those ROIs involved closely in working memory, attention, executive functions, and motor control. Moreover, the observation that tPBM enabled to strongly modulate myogenic oscillation within cerebral hemodynamic ISO across the human whole head is also highly consistent with our recent article (Wang et al, 2022). Accordingly, tPBM significantly enhanced the spectral amplitude of [HbO] in the myogenic bands by 23% near the tPBM site compared to the sham condition (Wang et al, 2022).…”

“…The report was based on dual-channel, bbNIRS measurements taken from a completely different group of participants and performed by different operators. Similarly, tPBM was reported to significantly enhance the spectral amplitude of [HbO] in the endogenic band by 13% near the tPBM site compared to the sham condition (Wang et al, 2022). The excellent agreement in observing tPBM-evoked strong modulation in endogenic oscillation between two independent studies strengthens the underlying physiological expectation that tPBM facilitates (either directly or indirectly) an increase in NO, which will trigger alterations in endogenic oscillations and then vasodilation within a period of 1-4 min.…”

Influence of the Signal-To-Noise Ratio on Variance of Chromophore Concentration Quantification in Broadband Near-Infrared Spectroscopy

“…In this study, we focus on the conventional NIRS with the wavelength range from 650 to 950 nm, which facilitates quantitative changes of the hemodynamic (Boas and Franceschini, 2011) and metabolic state of various tissue types, such as the breast (Cerussi et al, 2011;Jiang et al, 2013), muscle (Ferrari et al, 2011;Wang X. et al, 2016), or brain (Villringer et al, 1993;Smith, 2011;Tian et al, 2016;Wang et al, 2017;Pruitt et al, 2020;Wang et al, 2022). In this spectral range, the three main chromophores of interest in most NIRS-based studies are oxyhemoglobin (HbO), deoxyhemoglobin (HHb), and cytochrome-c-oxidase (CCO) (Heekeren et al, 1999;Kolyva et al, 2012;Bale et al, 2014;Kolyva et al, 2014;Wang X. et al, 2016;Wang et al, 2017;Wang et al, 2022). Numerous studies have revealed the potential use of NIRS in a wide range of clinical applications, including neuromonitoring (Lange and Tachtsidis, 2019;Pinti et al, 2020), metabolic state observation (Durduran et al, 2010;Hamaoka et al, 2011), or cancer detection (Nioka and Chance, 2005;Cerussi et al, 2011;Jiang et al, 2013).…”