Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine

Abstract

Migraine has been traditionally considered a nonprogressive, paroxysmal disorder with no brain abnormalities between attacks. We used diffusion tensor imaging to examine interictal diffusion properties of the brains of migraineurs with aura, migraineurs without aura and matched healthy controls. Areas of lower fractional anisotropy were present in migraineurs along the thalamocortical tract. In addition, migraineurs with aura had lower fractional anisotropy in the ventral trigeminothalamic tract, and migraineurs without aura had lower fractional anisotropy in the ventrolateral periaqueductal grey matter. Our results indicate the presence of permanent interictal changes in migraineurs, pointing to an effect of migraine on the trigeminal somatosensory and modulatory pain systems.

figure 1

Panels A, B and C show FA average significance maps superimposed on a T1 coronal section comparing migraine with aura (MWA, panel A), all migraine patients (MIG, panel B) and migraine without aura (MWoA, panel C) vs. healthy controls. Panels D, E and F show cuboid maps depicting the diffusion tensor within each voxel. The axes of each cube are placed regarding the main fibres orientation and are coloured accordingly: green indicates antero-posterior fibres; blue indicates supero-inferior fibres; and red indicates medio-lateral fibres. In panels D and F, cuboid maps are superimposed to the FA maps shown in panels A and C, respectively. The trigeminal somatosensory pathway scheme is represented in panel E. The rectangular areas in all panels focus the same anatomical structures. Significant lower FA values were noticed at the thalamocortical tract (3^rd order neurons) in both migraine subtypes. In addition, the trigeminothalamic tract (TTT) showed also significantly lower FA values in migraineurs with aura (panel A, lowest cluster inside the yellow square). In both migraine forms, FA clusters were located at the venteroposterior medial thalamic nucleus (VPM), extending upwards along the thalamocortical sensory pathway. The yellow-red shading code represents p values for lower FA changes. n=12 for MWA, MWoA and HC groups. SSC = somatosensory cortex. TNC = trigeminal nucleus caudalis.

figure 2

FA average significance maps comparing migraine with aura (MWA, left panel), and migraine without aura (MWoA, right panel) vs healthy controls (HC); and MWA vs. MWoA (middle panel). Significant changes were noticed in the trigeminothalamic tract (MWA vs. HC) and periaqueductal gray area (MWoA vs. HC). FA significant differences were also present between migraine subtypes. The yellow-red shading code represents p values for lower FA changes. The blue shading code represents p values for higher FA changes. n=12 for each group.