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Development of an EEG-fNIRS based online monitoring tool towards delivery of non-invasive brain stimulation

Authors:

Abstract

A method for electroencephalography (EEG)-functional near-infrared spectroscopy (fNIRS) based monitoring of cerebrobascular reactivity (CVR) and neurovascular coupling (NVC) during anodal transcranial direct current stimulation (tDCS) is presented. A case study on an able-bodied volunteer showed that our tDCS-fNIRS/EEG platform can characterize the “online” and “offline” effects of 2-mA tDCS modulation in both electrophysiological (EEG) and haemodynamic (fNIRS) components. Therefore, an EEG-fNIRS based online NVC/CVR monitoring tool towards delivery of non-invasive brain stimulation is proposed.
a)
b)
c)
Figure 1: a) Experimental setup of the High Definition (HD)-tDCS and
fNIRS/EEG probes/electrodes on the head. An 8-channel dual tDCS-
EEG system was used to deliver constant direct current (2mA: 20min) to
the left SMC via a 4x1 anodal HD-tDCS electrode montage (anode left
SMC (C3) and 4 cathodes as return electrodes). EEG was recorded at
500Hz from all 8 electrodes before and after HD-tDCS (Left: C3, FC1,
FC5, CP5, CP1, C1; Right: C4 and FC2), and from 3 electrodes during
HD-tDCS (Left: C1: Right: C4, and FC2). A multi channel fNIRS system
was used to continually measure at 10 Hz cortical haemodynamic
changes from 16 channels covering the bilateral sensorimotor network.
Locations of each of the 16 fNIRS channels (Left: 1-8; Right: 9-16) are
represented by a receiver-emitter combination. b) Resting-state fNIRS
(O2Hb-red traces; HHb-blue traces) during anodal HD-tDCS (2mA) for
first ~10 minutes. c) Spectrogram using short-time Fourier transform of
the resting-state eyes-open raw EEG at C1 (closest to C3 i.e. anode for
HD-tDCS) for first ~10 minutes during anodal HD-tDCS (2mA).
Abstract—A method for electroencephalography (EEG)-
functional near-infrared spectroscopy (fNIRS) based
monitoring of cerebrobascular reactivity (CVR) and
neurovascular coupling (NVC) during anodal transcranial
direct current stimulation (tDCS) is presented. A case study on
an able-bodied volunteer showed that our tDCS-fNIRS/EEG
platform can characterize the “online” and “offline” effects of
2-mA tDCS modulation in both electrophysiological (EEG) and
haemodynamic (fNIRS) components. Therefore, an EEG-fNIRS
based online NVC/CVR monitoring tool towards delivery of
non-invasive brain stimulation is proposed.
S
UMMARY
Cortical neural activity can be modulated with tDCS [1].
During cortical neural activity, the electric currents from all
excitable membranes of brain tissue superimpose in the
extracellular medium and generate EEG. Neural activity has
been shown to be closely related, spatially and temporally, to
cerebral blood flow (CBF) that supplies glucose via
neurovascular coupling (NVC) [2]. Here, cerebrovascular
reactivity (CVR) is the change in CBF in response to NVC
stimulus where its hemodynamic component can be captured
by functional near-infrared spectroscopy (fNIRS). fNIRS
(Oxymon MK III, Artinis Medical Systems) provided
continuous monitoring of cerebral oxygenation and blood
volume with high temporal resolution. We presented EEG-
fNIRS based monitoring of NVC/CVR under perturbation
with tDCS [3] where initial dip in the oxy-haemoglobin
concentration and concomitant increase in the mean power
spectral density within lower (<10Hz) frequency band were
observed. This initial transient of ~10sec duration in a stroke
patient who complained of headache during anodal tDCS
was much longer than that of other three stroke patients who
did not [3]. Therefore, we propose an EEG-fNIRS based
online monitoring tool for (impaired) dynamic cerebral
autoregulation towards online adaptation of non-invasive
brain stimulation (NIBS) parameters using MatNIC and
StarStim (Neuroelectrics, Spain) NIBS interface for (safe)
dosing of electrical stimulation, as illustrated in Figure 1.
*
Research supported by Franco-Indian INRIA-DST Associate Team
support 2014-2017, Franco-German PROCOPE, and M2H support.
A. Dutta is with the Institut national de recherche en informatique et en
automatique (INRIA), Montpellier, France (e-mail: adutta@ieee.org).
M. Muthalib is with the Movement To Health (M2H) Laboratory,
EUROMOV, Montpellier-1 University, Montpellier, France.
S. Roy Chowdhury is with the International Institute of Information
Technology, Hyderabad, India.
D. Guiraud is with the Institut national de recherche en informatique et
en automatique (INRIA), Montpellier, France.
M.A. Nitsche is with the University Medicine Goettingen, Germany.
S. Perrey is with the Movement To Health (M2H) Laboratory,
EUROMOV, Montpellier-1 University, Montpellier, France.
R
EFERENCES
[1] M. A. Nitsche and W. Paulus, “Excitability changes induced in the
human motor cortex by weak transcranial direct current
stimulation,” J. Physiol., vol. 527 Pt 3, pp. 633–639, Sep. 2000.
[2] H. Girouard and C. Iadecola, “Neurovascular coupling in the
normal brain and in hypertension, stroke, and Alzheimer disease,”
J. Appl. Physiol. 1985, vol. 100, no. 1, pp. 328–335, Jan. 2006.
[3] A. Dutta, “EEG-NIRS based low-cost screening and monitoring of
cerebral microvessels functionality,” International Stroke
Conference 2014, San Diego, 2014.
Development of an EEG-fNIRS based online monitoring tool
towards delivery of non-invasive brain stimulation
Anirban Dutta, Mark Muthalib, Shubhajit Roy Chowdhury, David Guiraud, Michael A. Nitsche,
Stephane Perrey
... Section "Discussion" summarizes and concludes with future directions. (19). eVidenCe in sUpport oF aLterations in CortiCaL eXCitation-inHiBition WitH non-inVasiVe CortiCaL and peripHeraL eLeCtriCaL stiMULation evidence from eeG-fMri studies with niBs A common practice that is followed during NIBS is the application is restricted to an isolated brain area. ...
... Here, the brain tissue serves as the scattering medium that allows NIR light detectors placed on the scalp to help estimate the chromophore's (in both arterial and venous blood) absorption using the Beer-Lambert law (18). Therefore, while EEG provides an electrophysiological measure of cortical neural activity, functional NIRS provides a measure of the related hemodynamic component that supplies glucose via NVC. Figure 1, adapted from Dutta et al. (19), shows an illustrative experimental setup. An eight-channel dual tDCS-EEG system (StarStim, Neuroelectrics, Spain) was used to deliver constant direct current (2 mA for 20 min) to the left sensorimotor cortex (SMC) via a 4 × 1 anodal High-Definition-tDCS (HD-tDCS) electrode montage with the anode at C3 (red circle in Figure 1) and surrounding four cathodes as return electrodes (blue circles in Figure 1). ...
... We propose an online tDCS adaptation system, called Brain State Dependent electrotherapy (BSDE) system, whose central aim is achieving E-I balance for therapeutic intervention (see Figure 8). The hemodynamic and electromagnetic variables corresponding to tDCS stimulation are estimated from the combined fNIRS and EEG system (as shown in Figure 5) using the framework developed by Dutta et al. (19). The Neural Mass Model system works as a generative model that takes the variables estimated from fNIRS and EEG such as ratio of oxygenated-todeoxygenated hemoglobin, band-specific power, event-related FiGUre 8 | adaptive Brain state dependent electrotherapy (Bsde). ...
Article
Full-text available
Stroke is the leading cause of severe chronic disability and the second cause of death worldwide with 15 million new cases and 50 million stroke survivors. The post stroke chronic disability may be ameliorated with early neurorehabilitation where non-invasive brain stimulation (NIBS) techniquescan be used as an adjuvant treatment to hasten the effects. However, the heterogeneity in the lesioned brain will require individualized NIBS intervention where innovative neuroimaging technologies of portable electroencephalography (EEG) and functional-near-infraredspectroscopy (fNIRS) can be leveraged for Brain State DependentElectrotherapy (BSDE). In this hypothesis and theory article, we propose a computational approach based on excitation-inhibition (E-I) balance hypothesis to objectively quantify the post stroke individual brain stateusing online fNIRS-EEG joint imaging. One of the key events that occurs following Stroke is the imbalance in local excitation-inhibition(that is the ratio of Glutamate/GABA) which may be targeted with NIBS using a computational pipeline that includes individual “forward models” to predictcurrent flow patterns through the lesioned brain or brain target region. The current flow will polarize the neurons which can be captured with excitation-inhibition based brain models. Furthermore, E-Ibalance hypothesis can be used to find the consequences of cellular polarization on neuronal informationprocessing which can then be implicated in changes in function. We first review evidence that shows how thislocal imbalance between excitation-inhibition leading to functional dysfunction can be restored in targeted sites with NIBS (Motor Cortex, Somatosensory Cortex) resulting in large scale plastic reorganization over the cortex, and probably facilitating recovery of functions. Secondly, we show evidence how BSDE based on inhibition–excitation balance hypothesis may target a specific brain site or network as an adjuvant treatment. Hence, computational neural mass modelbased integration of neurostimulation with online neuroimaging systems may provide less ambiguous,robust optimization of NIBS, and its application in neurological conditions and disorders acrossindividual patients.
... A multifunction off-the-shelf DAQ device (National Instruments Corporation, USA) can be used to provide basic physical input/output channels to drive the light sources and/or acquire optical signals. If the timing accuracy of DAQ is critical, e.g., for cross spectral analysis [42], then a real-time off-the-shelf DAQ system, such as CompactRIO or PXI (National Instruments Corporation, USA), is required. Usually, the analog output channels are limited in off-the-shelf DAQ devices (e.g., only 2 analog outputs in PCIe-6351 from National Instruments Corporation, USA) and therefore time division multiplexing technique can be used to illuminate light sources (light emitting diodes or laser diodes). ...
... A multifunction off-the-shelf DAQ device (National Instruments Corporation, USA) can be used to provide basic physical input/output channels to drive the light sources and/or acquire optical signals. If timing accuracy of DAQ is critical, e.g. for cross spectral analysis (Anirban Dutta 2014a), then a real-time offthe-shelf DAQ system, such as CompactRIO or PXI (National Instruments Corporation, USA), is required. Usually, the number of analog output channels are limited in off-the-shelf DAQ devices (e.g., only 2 analog outputs in PCIe-6351 from National Instruments Corporation, USA) and therefore the time division multiplexing technique can be used to illuminate multiple light sources (light emitting diodes or laser diodes). ...
Thesis
Full-text available
Transcranial direct current stimulation (tDCS) has been shown to modulate cortical neural activity (Nitsche and Paulus 2000). During neural activity, the electric currents from excitable membranes of brain tissue superimpose at a given location in the extracellular medium and generate a potential, which is referred to as the electroencephalogram (EEG) when recorded from the scalp (Nunez and Srinivasan 2006). Respective neural activity has been shown to be closely related, spatially and temporally, to cerebral blood flow (CBF) that supplies glucose via neurovascular coupling (Girouard and Iadecola 2006). The hemodynamic response to neural activity can be captured by near-infrared spectroscopy (NIRS), which enables continuous monitoring of cerebral oxygenation and blood volume (Siesler et al. 2008). Here, the CBF is increased in the brain regions with neural activity via metabolic coupling mechanisms (Attwell et al. 2010). Cerebral autoregulation mechanisms ensure that the blood flow is maintained during changes in the perfusion pressure (Lucas et al. 2010). We proposed a phenomological model for metabolic coupling mechanisms (Attwell et al. 2010) to capture cerebrovascular reactivity (CVR) that represented the capacity of blood vessels to dilate during anodal tDCS due to neuronal activity-caused increased demands of oxygen (Dutta et al. 2013). Crosssectional studies suggest that impaired cerebral hemodynamics precedes stroke and transient ischaemic attacks (TIA). CVR reflects the capacity of blood vessels to dilate, and is an important marker for brain vascular reserve (Markus and Cullinane 2001). Therefore, cerebrovascular reserve capacity may have a predictive value for the risk of cerebral infarction in patients with reduced cerebrovascular reserve capacity such that it might evolve as a part of routine diagnostic neuroangiologic program (Stoll and Hamann 2002).
... A multifunction offthe-shelf DAQ device (National Instruments Corporation, USA) can be used to provide basic physical input/output channels to drive the light sources and/or acquire optical signals. If the timing accuracy of DAQ is critical, e.g. for cross spectral analysis [42], then a real-time off-theshelf DAQ system, such as CompactRIO or PXI (National Instruments Corporation, USA), is required. Usually, the analog output channels are limited in off-the-shelf DAQ devices (e.g., only 2 analog outputs in PCIe-6351 from National Instruments Corporation, USA) and therefore time division multiplexing technique can be used to illuminate light sources (light emitting diodes or laser diodes). ...
Article
Full-text available
Objective: A method for electroencephalography (EEG) - near-infrared spectroscopy (NIRS) based assessment of neurovascular coupling (NVC) during anodal transcranial direct current stimulation (tDCS) is presented. Methods: Anodal tDCS modulates cortical neural activity leading to a hemodynamic response, which was used to identify impaired NVC functionality. In this study, the hemodynamic response was estimated with NIRS. NIRS recorded changes in oxy-hemoglobin ( ) and deoxy-hemoglobin ( ) concentrations during anodal tDCS-induced activation of the cortical region located under the electrode and in-between the light sources and detectors. Anodal tDCS-induced alterations in the underlying neuronal current generators were also captured with EEG. Then, a method for the assessment of NVC underlying the site of anodal tDCS was proposed that leverages the Hilbert-Huang Transform. Results: The case series including four chronic (>6 months) ischemic stroke survivors (3 males, 1 female from age 31 to 76) showed non-stationary effects of anodal tDCS on EEG that correlated with the response. Here, the initial dip in at the beginning of anodal tDCS corresponded with an increase in the log-transformed mean-power of EEG within 0.5Hz-11.25Hz frequency band. The cross-correlation coefficient changed signs but was comparable across subjects during and after anodal tDCS. The log-transformed mean-power of EEG lagged response during tDCS but then led post-tDCS. Conclusion: This case series demonstrates changes in the degree of neurovascular coupling to a 0.526A/m2 square-pulse (0-30sec) of anodal tDCS. The initial dip in needs to be carefully investigated in a larger cohort, for example in patients with small vessel disease.
... A multifunction offthe-shelf DAQ device (National Instruments Corporation, USA) can be used to provide basic physical input/output channels to drive the light sources and/or acquire optical signals. If the timing accuracy of DAQ is critical, e.g. for cross spectral analysis [42], then a real-time off-theshelf DAQ system, such as CompactRIO or PXI (National Instruments Corporation, USA), is required. Usually, the analog output channels are limited in off-the-shelf DAQ devices (e.g., only 2 analog outputs in PCIe-6351 from National Instruments Corporation, USA) and therefore time division multiplexing technique can be used to illuminate light sources (light emitting diodes or laser diodes). ...
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A method for electroencephalography (EEG) - near-infrared spectroscopy (NIRS) based assessment of neurovascular coupling (NVC) during anodal transcranial direct current stimulation (tDCS). Anodal tDCS modulates cortical neural activity leading to a hemodynamic response, which was used to identify impaired NVC functionality. In this study, the hemodynamic response was estimated with NIRS. NIRS recorded changes in oxy-hemoglobin (HbO2) and deoxy-hemoglobin (Hb) concentrations during anodal tDCS-induced activation of the cortical region located under the electrode and in-between the light sources and detectors. Anodal tDCS-induced alterations in the underlying neuronal current generators were also captured with EEG. Then, a method for the assessment of NVC underlying the site of anodal tDCS was proposed that leverages the Hilbert-Huang Transform. The case series including four chronic (>6 months) ischemic stroke survivors (3 males, 1 female from age 31 to 76) showed non-stationary effects of anodal tDCS on EEG that correlated with the HbO2 response. Here, the initial dip in HbO2 at the beginning of anodal tDCS corresponded with an increase in the log-transformed mean-power of EEG within 0.5Hz-11.25Hz frequency band. The cross-correlation coefficient changed signs but was comparable across subjects during and after anodal tDCS. The log-transformed mean-power of EEG lagged HbO2 response during tDCS but then led post-tDCS. This case series demonstrated changes in the degree of neurovascular coupling to a 0.526 A/m(2) square-pulse (0-30 s) of anodal tDCS. The initial dip in HbO2 needs to be carefully investigated in a larger cohort, for example in patients with small vessel disease.
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In this paper we demonstrate in the intact human the possibility of a non-invasive modulation of motor cortex excitability by the application of weak direct current through the scalp. Excitability changes of up to 40 %, revealed by transcranial magnetic stimulation, were accomplished and lasted for several minutes after the end of current stimulation. Excitation could be achieved selectively by anodal stimulation, and inhibition by cathodal stimulation. By varying the current intensity and duration, the strength and duration of the after-effects could be controlled. The effects were probably induced by modification of membrane polarisation. Functional alterations related to post-tetanic potentiation, short-term potentiation and processes similar to postexcitatory central inhibition are the likely candidates for the excitability changes after the end of stimulation. Transcranial electrical stimulation using weak current may thus be a promising tool to modulate cerebral excitability in a non-invasive, painless, reversible, selective and focal way.
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