Abstract
The process of neurovascular coupling ensures that increases in neuronal activity are fed by increases in cerebral blood flow. Evidence suggests that neurovascular coupling may be impaired in Multiple Sclerosis (MS) due to a combination of brain hypoperfusion, altered cerebrovascular reactivity and oxygen metabolism, and altered levels of vasoactive compounds.Here, we tested the hypothesis that neurovascular coupling is impaired in MS. We characterized neurovascular coupling as the relationship between changes in neuronal oscillatory power within the gamma frequency band (30–80 Hz), as measured by magnetoencephalography (MEG), and associated hemodynamic changes (blood oxygenation level dependent, BOLD, and cerebral blood flow, CBF) as measured by functional MRI. We characterized these responses in the visual cortex in 13 MS patients and in 10 matched healthy controls using a reversing checkerboard stimulus at five visual contrasts.There were no significant group differences in visual acuity, P100 latencies, occipital gray matter (GM) volumes and baseline CBF. However, in the MS patients we found a significant reduction in peak gamma power, BOLD and CBF responses. There were no significant differences in neurovascular coupling between groups, in the visual cortex.Our results suggest that neuronal and vascular responses are altered in MS. Gamma power reduction could be an indicator of GM dysfunction, possibly mediated by GABAergic changes. Altered hemodynamic responses confirm previous reports of a vascular dysfunction in MS. Despite altered neuronal and vascular responses, neurovascular coupling appears to be preserved in MS, at least within the range of damage and disability studied here.
Highlights
Neuronal activity and cerebral blood flow (CBF) have a close spatial and temporal relationship: increases in neuronal activity are associated with local increases in CBF via changes in blood vessel tone, a process known as neurovascular coupling
We investigated neurovascular coupling in Multiple Sclerosis (MS) using two complementary non-invasive imaging modalities: magnetoencephalography (MEG) and functional Magnetic Resonance Imaging. fMRI signals are based on the local vascular response, a process known as functional hyperaemia
The group region of interest (ROI) consisted of common significant voxels among blood oxygen-level-dependent (BOLD) activity in the control group, BOLD activity in the patient group, CBF activity in the control group and CBF activity in the patient group
Summary
Neuronal activity and cerebral blood flow (CBF) have a close spatial and temporal relationship: increases in neuronal activity are associated with local increases in CBF via changes in blood vessel tone, a process known as neurovascular coupling. In Multiple Sclerosis, hypoperfusion is seen in both GM and normal appearing WM (Swank et al, 1982; Brooks et al, 1984; Lycke et al, 1993; Sun et al, 1998; Law et al, 2004; Adhya et al, 2006; D’haeseleer et al, 2013), as well as reports of impaired vascular reactivity (Marshall et al, 2014, 2016) and reduced oxygen metabolism (Ge et al, 2012) Vasoactive agents such as nitric oxide and endothelin-1 that have profound, and often contrasting, effects on the vasculature are significantly raised within MS lesions Glial cells have a key role in responding to damage in the MS brain, as well as playing a crucial role in neurovascular coupling (Metea and Newman, 2006) The combination of these factors may lead to an alteration of the hemodynamic response to neuronal activity in MS, the hypothesis tested in this study. The patient group presented with more varied neurovascular coupling relationships than the controls, but there was no significant group difference in neurovascular coupling, in the early visual cortex
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