Arterial blood stealing as a mechanism of negative BOLD response: From the steady-flow with nonlinear phase separation to a windkessel-based model

Suarez, Alejandro L.; Valdés-Hernández, Pedro A.; Moshkforoush, Arash; Tsoukias, Nikolaos M.; Riera, Jorge J.

doi:10.1016/j.jtbi.2021.110856

Cited by 3 publications

(3 citation statements)

References 53 publications

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“…In addition, prolonged somatosensory stimulations drive a decline in EEG activity and reduce CBF in the neonatal mouse ( Zehendner et al, 2013 ), suggesting the inability to sustain neural processing during prolonged stimulations in the immature brain. The decrease in CBF may also be due to redistribution and hence ‘haemodynamic steal’ of blood towards an adjacent cortical region of neuronal activity ( Kozberg and Hillman, 2016 ; Suarez et al, 2021 ). In contrast, prolonged stimulation in adult mice was associated with stable neural processing and increased regional CBF.…”

Section: Discussionmentioning

confidence: 99%

Cerebral haemodynamic response to somatosensory stimulation in preterm lambs is enhanced following sildenafil and inhaled nitric oxide administration

et al. 2023

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Background: Neurovascular coupling (NVC) leads to an increase in local cerebral blood flow and oxygenation in response to increased neural activity and metabolic demand. Impaired or immature NVC reported in the preterm brain, potentially reduces cerebral oxygenation following increased neural activity, predisposing to cerebral tissue hypoxia. Endogenous nitric oxide (NO) is a potent vasodilator and a major mediator of NVC and the cerebral haemodynamic response. NO modulators, such as inhaled nitric oxide (iNO) and sildenafil, induce vasodilation and are used clinically to treat pulmonary hypertension in preterm neonates. However, their impact on NVC in the preterm brain are unknown. We aimed to characterise the cerebral functional haemodynamic response in the preterm brain exposed to NO modulators. We hypothesized that iNO and sildenafil in clinical dosages would increase the baseline cerebral perfusion and the cerebral haemodynamic response to neural activation.Methods: Preterm lambs (126–7 days’ gestation) were delivered and mechanically ventilated. The cerebral functional haemodynamic response was measured using near infrared spectroscopy as changes in cerebral oxy- and deoxyhaemoglobin (ΔoxyHb, ΔdeoxyHb), following left median nerve stimulations of 1.8, 4.8, and 7.8 s durations in control preterm lambs (n = 11), and following 4.8 and 7.8 s stimulations in preterm lambs receiving either sildenafil citrate (n = 6, 1.33 mcg/kg/hr) or iNO (n = 8, 20 ppm).Results: Following 1.8, 4.8, and 7.8 s stimulations, ∆oxyHb in the contralateral cortex increased (positive functional response) in 7/11 (64%), 7/11 (64%), and 4/11 (36%) control lambs respectively (p < 0.05). Remaining lambs showed decreased ΔoxyHb (negative functional response). Following 4.8 s stimulations, more lambs receiving sildenafil or iNO (83% and 100% respectively) showed positive functional response compared to the controls (p < 0.05). No significant difference between the three groups was observed at 7.8 s stimulations.Conclusion: In the preterm brain, prolonged somatosensory stimulations increased the incidence of negative functional responses with decreased cerebral oxygenation, suggesting that cerebral oxygen delivery may not match the oxygen demand. Sildenafil and iNO increased the incidence of positive functional responses, potentially enhancing NVC, and cerebral oxygenation.

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Section: Discussionmentioning

confidence: 99%

Cerebral haemodynamic response to somatosensory stimulation in preterm lambs is enhanced following sildenafil and inhaled nitric oxide administration

et al. 2023

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“…A viscoelastic nonlinear delayed compliance was also included (54). To account for blood stealing effects in brain regions sharing a common supply artery (Option 1, Supplementary Table A1), an inductive element was added to connect their respective Windkessel components (39). For regions not sharing a common supplying artery, the two equations for the CBF become independent.…”

Section: The Biophysical Modelmentioning

confidence: 99%

“…Also, an initial work by Harel et al (38) suggested that arterial blood stealing (ABS) could cause an NBR in healthy brain areas as a result of decreases in cerebral blood flow (CBF) and volume (CBV) in a region in close proximity to an IED-evoked PBR. A recent computational model (39) demonstrated that ABS is physically possible in the brain vasculature. More recent studies have corroborated experimentally the existence of ABS (40,41).…”

Section: Introductionmentioning

confidence: 99%

Identification of Negative BOLD Responses in Epilepsy Using Windkessel Models

et al. 2021

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Alongside positive blood oxygenation level–dependent (BOLD) responses associated with interictal epileptic discharges, a variety of negative BOLD responses (NBRs) are typically found in epileptic patients. Previous studies suggest that, in general, up to four mechanisms might underlie the genesis of NBRs in the brain: (i) neuronal disruption of network activity, (ii) altered balance of neurometabolic/vascular couplings, (iii) arterial blood stealing, and (iv) enhanced cortical inhibition. Detecting and classifying these mechanisms from BOLD signals are pivotal for the improvement of the specificity of the electroencephalography–functional magnetic resonance imaging (EEG-fMRI) image modality to identify the seizure-onset zones in refractory local epilepsy. This requires models with physiological interpretation that furnish the understanding of how these mechanisms are fingerprinted by their BOLD responses. Here, we used a Windkessel model with viscoelastic compliance/inductance in combination with dynamic models of both neuronal population activity and tissue/blood O2 to classify the hemodynamic response functions (HRFs) linked to the above mechanisms in the irritative zones of epileptic patients. First, we evaluated the most relevant imprints on the BOLD response caused by variations of key model parameters. Second, we demonstrated that a general linear model is enough to accurately represent the four different types of NBRs. Third, we tested the ability of a machine learning classifier, built from a simulated ensemble of HRFs, to predict the mechanism underlying the BOLD signal from irritative zones. Cross-validation indicates that these four mechanisms can be classified from realistic fMRI BOLD signals. To demonstrate proof of concept, we applied our methodology to EEG-fMRI data from five epileptic patients undergoing neurosurgery, suggesting the presence of some of these mechanisms. We concluded that a proper identification and interpretation of NBR mechanisms in epilepsy can be performed by combining general linear models and biophysically inspired models.

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Cortical Activation in Response to Speech Differs between Prelingually Deafened Cochlear Implant Users with Good or Poor Speech-in-Noise Understanding: An fNIRS Study

2022

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Cochlear implant (CI) users with prelingual deafness (hearing impairment started before language development was completed) show variable speech-in-noise (SIN) understanding. The present study aimed to assess cortical activation patterns to speech-in-quiet (SIQ) and SIN in prelingual CI users and compared to individuals with normal hearing (NH), using functional Near-Infrared Spectroscopy (fNIRS). Participants included 15 NH who listened to natural speech, 15 NH who listened via 8-channel noise-excited vocoder, and 14 prelingual CI users. fNIRS data were collected in a block design that included three conditions: SIQ, SIN in a signal-to-noise ratio of 0 dB, and noise. Speech reception thresholds in noise (SRTn) were also assessed. Results revealed different patterns of activation between the NH and CI participants in channels covering mainly the right and left middle temporal gyrus (MTG), depending on the SRTn of the CI users. Specifically, while the NH group showed large response to SIQ and SIN in the MTG areas, prelingual CI users with poor SRTn showed significantly smaller response to SIQ, and inversed response (a reduction in activation) to SIN in the same brain areas. These novel findings support the notion that the MTG can serve as a neural marker for speech understanding in CI patients.

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Arterial blood stealing as a mechanism of negative BOLD response: From the steady-flow with nonlinear phase separation to a windkessel-based model

Cited by 3 publications

References 53 publications

Cerebral haemodynamic response to somatosensory stimulation in preterm lambs is enhanced following sildenafil and inhaled nitric oxide administration

Cerebral haemodynamic response to somatosensory stimulation in preterm lambs is enhanced following sildenafil and inhaled nitric oxide administration

Identification of Negative BOLD Responses in Epilepsy Using Windkessel Models

Cortical Activation in Response to Speech Differs between Prelingually Deafened Cochlear Implant Users with Good or Poor Speech-in-Noise Understanding: An fNIRS Study

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