Non-invasive, multimodal analysis of cortical activity, blood volume and neurovascular coupling in infantile spasms using EEG-fNIRS monitoring

Abstract

Although infantile spasms can be caused by a variety of etiologies, the clinical features are stereotypical. The neuronal and vascular mechanisms that contribute to the emergence of infantile spasms are not well understood. We performed a multimodal study by simultaneously recording electroencephalogram and functional Near-infrared spectroscopy in an intentionally heterogeneous population of six children with spasms in clusters. Regardless of the etiology, spasms were accompanied by two phases of hemodynamic changes; an initial change in the cerebral blood volume (simultaneously with each spasm) followed by a neurovascular coupling in all children except for the one with a large porencephalic cyst. Changes in cerebral blood volume, like the neurovascular coupling, occurred over frontal areas in all patients regardless of any brain damage suggesting a diffuse hemodynamic cortical response. The simultaneous motor activation and changes in cerebral blood volume might result from the involvement of the brainstem. The inconstant neurovascular coupling phase suggests a diffuse activation of the brain likely resulting too from the brainstem involvement that might trigger diffuse changes in cortical excitability.

Neurovascular coupling in the developing neonatal brain at rest

“…The changes in HbO–HbR demonstrated by multidistance NIRS analysis support the idea that hemodynamic changes are the result of changes in the dynamics of cortical microvessels. The laser hemodynamic response supports pollution (or cross‐talk) from deeper structures that progressively disappear from deep to superficial layers (Bourel‐Ponchel et al, ).…”

“…However, some studies did not observe typical NVC and many studies have reported negative NVC in response to exogenous stimulation (A. P. Born et al, ). Apart from the immaturity of intimate cellular mechanisms, these differences could also be due to the different strategies of the vascular system to respond to increased metabolic demand, depending on baseline status of the neuronal and hemodynamic system (Bourel‐Ponchel, Mahmoudzadeh, Delignières, Berquin, & Wallois, ). According to the classification based on hemodynamic response, averaging of the various responses will obviously modify the global averaged hemodynamic output comprising a mix of positive and negative CBF or CBV responses, resulting in the absence of a hemodynamic response observed in Subcondition A0 without taking into account the IBI or the direction of HbO and HbR changes.…”

“…A linear correlation was observed between the RMS of neuronal EEG activity and the RMS of the hemodynamic response, despite the possible implication of the subplate neurons and other nonsynchronized or poorly orientated pyramidal cells, which might participate in the elaboration of the type of neurovascular response triggered by the underlying neuronal activity (cortical plate or subplate). In addition, other nonoxidative metabolic mechanisms are likely to participate (Bourel‐Ponchel et al, ). However, in a nonlinear investigation, the predominant driving influence of EEG on NIRS‐DCS (or the inverse) differed in the various preterm neonates.…”

“…Alternatively, an inverted NVC related to a situation of anaerobic metabolism has been proposed to explain the hemodynamic response to epileptic spasms associated with metabolic dysfunction treated by a ketogenic diet only (Bourel‐Ponchel et al, ). The negative NIRS seems to be driven by decreased CBF.…”

“…However, some studies did not observe typical NVC and many studies have reported negative NVC in response to exogenous stimulation (A. P. Born et al, 2000). Apart from the immaturity of intimate cellular mechanisms, these differences could also be due to the different strategies of the vascular system to respond to increased metabolic demand, depending on baseline status of the neuronal and hemodynamic system (Bourel-Ponchel, Mahmoudzadeh, Delignières, Berquin, & Wallois, 2017).…”