Multispectral brain connectivity during visual attention distinguishes controlled from uncontrolled hypertension

Author:

Son Jake J.12ORCID,Arif Yasra1,Oludipe Davina1,Weyrich Lucas13,Killanin Abraham D.12,Wiesman Alex I.4,Okelberry Hannah J.1,Willett Madelyn P.1,Johnson Hallie J.1,Wilson Tony W.123ORCID

Affiliation:

1. Institute for Human Neuroscience Boys Town National Research Hospital Boys Town NE USA

2. College of Medicine University of Nebraska Medical Center Omaha NE USA

3. Department of Pharmacology & Neuroscience Creighton University Omaha NE USA

4. Montreal Neurological Institute McGill University Montreal QC Canada

Abstract

AbstractHypertension‐related changes in brain function place individuals at higher risk for cognitive impairment and Alzheimer's disease. The existing functional neuroimaging literature has identified important neural and behavioural differences between normotensive and hypertensive individuals. However, previously‐used methods (i.e. magnetic resonance imaging, functional near‐infrared spectroscopy) rely on neurovascular coupling, which is a useful but indirect measure of neuronal activity. Furthermore, most studies fail to distinguish between controlled and uncontrolled hypertensive individuals, who exhibit significant behavioural and clinical differences. To partially remedy this gap in the literature, we used magnetoencephalography (MEG) to directly examine neuronal activity that is invariant to neurovascular coupling changes induced by hypertension. Our study included 52 participants (19 healthy controls, 15 controlled hypertensives, 18 uncontrolled hypertensives) who completed a modified flanker attention task during MEG. We identified significant oscillatory neural responses in two frequencies (alpha: 8–14 Hz, gamma: 48–60 Hz) for imaging and used grand‐averaged images to determine seeds for whole‐brain connectivity analysis. We then conducted Fisher‐z tests for each pair of groups, using the relationship between the neural connectivity and behavioural attention effects. This highlighted a distributed network of regions associated with cognitive control and selective attention, including frontal‐occipital and interhemispheric occipital connections. Importantly, the inferior frontal cortex exhibited a unique neurobehavioural relationship that distinguished the uncontrolled hypertensive group from the controlled hypertensive and normotensive groups. This is the first investigation of hypertension using MEG and identifies critical whole‐brain connectivity differences based on hypertension profiles. imageKey points Structural and functional changes in brain circuitry scale with hypertension severity and increase the risk of cognitive impairment and Alzheimer's disease. We harness the excellent spatiotemporal precision of magnetoencephalography (MEG) to directly quantify dynamic functional connectivity in healthy control, controlled hypertensive and uncontrolled hypertensive groups during a flanker task. In the first MEG study of hypertension, we show that there are neurobehavioural relationships that distinguish the uncontrolled hypertensive group from healthy and controlled hypertensive group in the prefrontal cortex. These results provide novel insights into the differential impact of hypertension on brain dynamics underlying selective attention.

Funder

American Heart Association

National Institutes of Health

Publisher

Wiley

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