Photosensitive epilepsy is associated with reduced inhibition of alpha rhythm generating networks.
See Hamandi (doi:10.1093/awx049) for a scientific commentary on this article.Photosensitivity is a condition in which lights induce epileptiform activities. This abnormal electroencephalographic response has been associated with hyperexcitability of the visuo-motor system. Here, we evaluate if intrinsic dysfunction of this network is present in brain activity at rest, independently of any stimulus and of any paroxysmal electroencephalographic activity. To address this issue, we investigated the haemodynamic correlates of the spontaneous alpha rhythm, which is considered the hallmark of the brain resting state, in photosensitive patients and in people without photosensitivity. Second, we evaluated the whole-brain functional connectivity of the visual thalamic nuclei in the various populations of subjects under investigation. Forty-four patients with epilepsy and 16 healthy control subjects underwent an electroencephalography-correlated functional magnetic resonance imaging study, during an eyes-closed condition. The following patient groups were included: (i) genetic generalized epilepsy with photosensitivity, 16 subjects (mean age 25 ± 10 years); (ii) genetic generalized epilepsy without photosensitivity, 13 patients (mean age 25 ± 11 years); (iii) focal epilepsy, 15 patients (mean age 25 ± 9 years). For each subject, the posterior alpha power variations were convolved with the standard haemodynamic response function and used as a regressor. Within- and between-groups second level analyses were performed. Whole brain functional connectivity was evaluated for two thalamic regions of interest, based on the haemodynamic findings, which included the posterior thalamus (pulvinar) and the medio-dorsal thalamic nuclei. Genetic generalized epilepsy with photosensitivity demonstrated significantly greater mean alpha-power with respect to controls and other epilepsy groups. In photosensitive epilepsy, alpha-related blood oxygen level-dependent signal changes demonstrated lower decreases relative to all other groups in the occipital, sensory-motor, anterior cingulate and supplementary motor cortices. Coherently, the same brain regions demonstrated abnormal connectivity with the visual thalamus only in epilepsy patients with photosensitivity. As predicted, our findings indicate that the cortical-subcortical network generating the alpha oscillation at rest is different in people with epilepsy and visual sensitivity. This difference consists of a decreased alpha-related inhibition of the visual cortex and sensory-motor networks at rest. These findings represent the substrate of the clinical manifestations (i.e. myoclonus) of the photoparoxysmal response. Moreover, our results provide the first evidence of the existence of a functional link between the circuits that trigger the visual sensitivity phenomenon and those that generate the posterior alpha rhythm.
Department of Biomedical, Metabolic, and Neural Science, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, OCSE Hospital, Modena, Italy.|Neurology Unit, OCSAE Hospital, Azienda Ospedaliera Universitaria, Modena, Italy.
Anna Elisabetta
AE
Vaudano
Department of Biomedical, Metabolic, and Neural Science, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, OCSE Hospital, Modena, Italy.|Neurology Unit, OCSAE Hospital, Azienda Ospedaliera Universitaria, Modena, Italy.
Andrea
A
Ruggieri
Department of Neuroscience, University of Parma, Consiglio nazionale delle Ricerche - CNR, Parma, Italy.
Pietro
P
Avanzini
Neurology Unit, OCSAE Hospital, Azienda Ospedaliera Universitaria, Modena, Italy.
Giuliana
G
Gessaroli
Department of Life and Reproduction Sciences, University of Verona, Verona, Italy.
Gaetano
G
Cantalupo
Epilepsy Centre, Department of Neuroscience, Odontostomatology and Reproductive Sciences, Federico II University, Naples, Italy.
Antonietta
A
Coppola
Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, National Hospital for Neurology and Neurosurgery, LondonWC1N 3BG, UK.|Epilepsy Society, Chalfont-St-Peter, Bucks SL9 0RJ, UK.
Sanjay M
SM
Sisodiya
Department of Biomedical, Metabolic, and Neural Science, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, OCSE Hospital, Modena, Italy.|Neurology Unit, OCSAE Hospital, Azienda Ospedaliera Universitaria, Modena, Italy.
Stefano
S
Meletti
D000293:Adolescent; D000328:Adult; D000513:Alpha Rhythm / Q000235:genetics; D001921:Brain / Q000000981:diagnostic imaging / Q000503:physiopathology; D004569:Electroencephalography; D004828:Epilepsies, Partial / Q000000981:diagnostic imaging / Q000503:physiopathology; D004829:Epilepsy, Generalized / Q000000981:diagnostic imaging / Q000503:physiopathology; D020195:Epilepsy, Reflex / Q000000981:diagnostic imaging / Q000235:genetics / Q000503:physiopathology*; D005260:Female; D006439:Hemodynamics; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009415:Nerve Net / Q000000981:diagnostic imaging / Q000503:physiopathology*; D010100:Oxygen / Q000097:blood; D012146:Rest; D012189:Retrospective Studies; D013787:Thalamic Nuclei / Q000000981:diagnostic imaging / Q000503:physiopathology; D055815:Young Adult
D010100:Oxygen
BOLD; alpha rhythm; epilepsy; functional connectivity; photosensitivity