Epilepsy-related brain networks in ring chromosome 20 syndrome: An EEG-fMRI study

Authors

  • Anna Elisabetta Vaudano,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
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    • The authors contributed equally to the work.
  • Andrea Ruggieri,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
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    • The authors contributed equally to the work.
  • Aglaia Vignoli,

    1. Department of Health Science, Epilepsy Center, San Paolo Hospital, University of Milan, Milan, Italy
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  • Pietro Avanzini,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
    2. Department of Neuroscience, University of Parma, Parma, Italy
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  • Francesca Benuzzi,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
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  • Giuliana Gessaroli,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
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  • Paolo Frigio Nichelli,

    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
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  • Francesca Darra,

    1. Department of Life and Reproduction Sciences, University of Verona, Verona, Italy
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  • Gaetano Cantalupo,

    1. Department of Life and Reproduction Sciences, University of Verona, Verona, Italy
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  • Massimo Mastrangelo,

    1. Pediatric Neurology Unit, V. Buzzi Hospital, A.O. ICP, Milano, Italy
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  • Bernardo Dalla Bernardina,

    1. Department of Life and Reproduction Sciences, University of Verona, Verona, Italy
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  • Maria Paola Canevini,

    1. Department of Health Science, Epilepsy Center, San Paolo Hospital, University of Milan, Milan, Italy
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  • Stefano Meletti

    Corresponding author
    1. Department of Biomedical Sciences, Metabolic, and Neuroscience, NOCSAE Hospital, University of Modena and Reggio Emilia, Modena, Italy
    • Address correspondence to Stefano Meletti, Department of Biomedical Sciences, Metabolic, and Neuroscience; University of Modena and Reggio Emilia, NOCSAE Hospital, via Giardini 1355, 41126 Modena, Italy. E-mail: stefano.meletti@unimore.it

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Summary

Objective

To identify the brain networks that are involved in the different electroencephalography (EEG) abnormalities in patients with ring chromosome 20 [r(20)] syndrome. We hypothesize the existence of both distinctive and common brain circuits for the paroxysmal high voltage sharp waves (hSWs), the seizures, and the slow-wave 3–7 Hz rhythm that characterize this condition.

Methods

Thirteen patients with [r(20)] syndrome were studied by means of EEG simultaneously recorded with functional magnetic resonance imaging (EEG-fMRI). EEG traces were reviewed in order to detect the pathologic interictal (hSWs) and ictal activities; the 3–7 Hz theta-delta power was derived using a fast Fourier transform. A group-level analysis was performed for each type of EEG abnormality separately using a fixed-effect model and a conjunction analysis. Finally, a second-level random-effect model was applied considering together the different EEG abnormalities, without distinction between hSW, seizures, or theta-delta rhythms.

Results

Subcontinuous theta-delta rhythm was recorded in seven patients, seizures in two, and hSWs in three patients. The main results are the following: (1) the slow-wave rhythm was related to blood oxygen level–dependent (BOLD) increases in the premotor, sensory-motor, and temporoparietal cortex, and to BOLD decrements involving the default mode (DMN) and the dorsal attention networks (DANs); (2) the ictal-related BOLD changes showed an early involvement of the prefrontal lobe; (3) increases in BOLD signal over the basal ganglia, either for interictal and ictal activities, were observed; (4) a common pattern of positive BOLD changes in the bilateral perisylvian regions was found across the different EEG abnormalities.

Significance

The BOLD increment in the perisylvian network and the decrease of the DMN and DAN could be the expression of the [r(20)] syndrome–related cognitive and behavioral deficits. The observed BOLD patterns are similar to the ones detected in other epileptic encephalopathies, suggesting that different epileptic disorders characterized by neurobehavioral regression are associated with dysfunction in similar brain networks.

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