Topiramate modulates trigeminal pain processing in thalamo-cortical networks in humans after single dose administration

TY - JOUR

T1 - Topiramate modulates trigeminal pain processing in thalamo-cortical networks in humans after single dose administration

AU - Hebestreit, Julia M

AU - May, Arne

PY - 2017

Y1 - 2017

N2 - Migraine is the sixth most common cause of disability in the world. Preventive migraine treatment is used to reduce frequency, severity and duration of attacks and therefore lightens the burden on the patients' quality of life and reduces disability. Topiramate is one of the preventive migraine treatments of proven efficacy. The mechanism of action underlying the preventive effect of topiramate in migraine remains largely unknown. Using functional magnetic resonance imaging (fMRI) we examined the central effects of a single dose of topiramate (100mg) on trigeminal pain in humans, compared to placebo (mannitol). In this prospective, within subject, randomized, placebo-controlled and double-blind study, 23 healthy participants received a standardized nociceptive trigeminal stimulation and control stimuli whilst being in the scanner. No differences in the subjective intensity ratings of the painful stimuli were observed between topiramate and placebo sessions. In contrast, topiramate significantly decreased the activity in the thalamus and other pain processing areas. Additionally, topiramate increased functional coupling between the thalamus and several brain regions such as the bilateral precuneus, posterior cingulate cortex and secondary somatosensory cortex. These data suggest that topiramate exhibits modulating effects on nociceptive processing in thalamo-cortical networks during trigeminal pain and that the preventive effect of topiramate on frequent migraine is probably mediated by an effect on thalamo-cortical networks.

AB - Migraine is the sixth most common cause of disability in the world. Preventive migraine treatment is used to reduce frequency, severity and duration of attacks and therefore lightens the burden on the patients' quality of life and reduces disability. Topiramate is one of the preventive migraine treatments of proven efficacy. The mechanism of action underlying the preventive effect of topiramate in migraine remains largely unknown. Using functional magnetic resonance imaging (fMRI) we examined the central effects of a single dose of topiramate (100mg) on trigeminal pain in humans, compared to placebo (mannitol). In this prospective, within subject, randomized, placebo-controlled and double-blind study, 23 healthy participants received a standardized nociceptive trigeminal stimulation and control stimuli whilst being in the scanner. No differences in the subjective intensity ratings of the painful stimuli were observed between topiramate and placebo sessions. In contrast, topiramate significantly decreased the activity in the thalamus and other pain processing areas. Additionally, topiramate increased functional coupling between the thalamus and several brain regions such as the bilateral precuneus, posterior cingulate cortex and secondary somatosensory cortex. These data suggest that topiramate exhibits modulating effects on nociceptive processing in thalamo-cortical networks during trigeminal pain and that the preventive effect of topiramate on frequent migraine is probably mediated by an effect on thalamo-cortical networks.

KW - Adult

KW - Double-Blind Method

KW - Female

KW - Fructose

KW - Gyrus Cinguli

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Migraine Disorders

KW - Neuroprotective Agents

KW - Pain

KW - Placebo Effect

KW - Prospective Studies

KW - Somatosensory Cortex

KW - Thalamus

KW - Young Adult

KW - Journal Article

KW - Randomized Controlled Trial

U2 - 10.1371/journal.pone.0184406

DO - 10.1371/journal.pone.0184406

M3 - SCORING: Journal article

C2 - 28991914

VL - 12

SP - e0184406

JO - PLOS ONE

JF - PLOS ONE

SN - 1932-6203

IS - 10

ER -