Somatosensory migraine auras evoked by bihemispheric cortical spreading depression events in human parietal cortex

Abstract

Cortical spreading depression (CSD) is associated with pronounced alterations in cerebral blood flow. These alterations can be captured using high-field functional magnetic resonance imaging (fMRI). While compelling clinical and experimental data suggest that CSD is involved in the pathogenesis of migraine aura, the mechanistic intricacies remain poorly understood. Here, we use visual stimulus-induced blood oxygen level-dependent (BOLD) fMRI responses to characterize spatiotemporal alterations in cerebral blood flow during spontaneous attacks with migraine aura. Six adult participants diagnosed with migraine with aura underwent BOLD fMRI scans with a visual stimulation paradigm, consisting of flickering checkerboard stimulation. Our results revealed that auras with somatosensory symptoms corresponded with bilateral alterations of stimulus-induced BOLD responses in the somatosensory cortex, exhibiting anterior-to-posterior propagation and absence of antecedent occipital abnormalities. These altered stimulus-induced BOLD responses were bilateral, despite a unilateral manifestation of aura symptoms, and had no relationship with positive or negative aura symptoms. The bilateral abnormalities in stimulus-induced BOLD responses completes our current knowledge on migraine aura.

Keywords: Aura; BOLD; cortical spreading depression; fMRI; migraine.

Figure 1.

BOLD imaging of migraine aura with visual and somatosensory symptoms. (a) Participant 1. Visual and sensory aura scanned 9 minutes after onset. Increased response (red colour) to visual stimulation within occipital, posterior cingulate and pre-frontal cortices and a mild decreased response (blue colour) in right calcarine cortex. (b) Participant 2. Lingual cortex shows decreased response bilaterally 17 minutes post visual aura onset, along with bilateral V3V hyperexcitability. Bilateral insula and lateral somatosensory cortex hyper excitability was observed before sensory aura with a mild delayed increased response of somatosensory cortex during the sensory aura and (c) Participant 3. Triggered sensory and visual aura. Increased response (red) of lateral somatosensory cortex at onset of sensory aura, spreading to occipital lobe at onset of visual aura, leaving a decreased response (blue) at the end of the symptoms.

Figure 2.

BOLD imaging of migraine aura with visual symptoms. (a) Participant 4. A long-lasting visual aura, captured 4 hours post-onset, demonstrated decreased response (blue colour) of the visual cortex, centered on the right and left cuneus and calcarine cortex. (b) Participant 5. A right lingual cortex increased response (hot colours) and a decreased response of the left calcarine cortex (cold colours) were observed 25 minutes after the onset of visual aura spreading to the left visual field and (c) Participant 6. Decreased response of bilateral lingual cortex (blue) and increased response of bilateral cuneus (red), 22 minutes after onset of scotoma lateralized to the left.