Integrity of corpus callosum is essential for the cross-hemispheric propagation of sleep slow waves: a high-density EEG study in split-brain patients

Giulia Avvenuti, Giacomo Handjaras, Monica Betta, Jacinthe Cataldi, Laura Sophie Imperatori, Simona Lattanzi, Brady Riedner, Pietro Pietrini, Emiliano Ricciardi, Giulio Tononi, Francesca Siclari, Gabriele Polonara, Mara Fabri, Mauro Silvestrini, Michele Bellesi, Giulio Bernardi

Research output: Contribution to journalArticle (Academic Journal)peer-review

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Abstract

The slow waves of NREM-sleep reflect experience-dependent plasticity and play a direct role in the restorative functions of sleep. Importantly, slow waves behave as traveling waves and their propagation is assumed to occur through cortico-cortical white matter connections. In this light, the corpus callosum (CC) may represent the main responsible for cross-hemispheric slow wave propagation. To verify this hypothesis, we performed overnight hd-EEG recordings in five patients who underwent total callosotomy due to drug-resistant epilepsy (CP; 2 females), in three non-callosotomized neurological patients (NP; 2 females), and in sample of 24 healthy adult subjects (HS; 13 females). In all CP slow waves displayed a significantly reduced probability of cross-hemispheric propagation and a stronger inter-hemispheric asymmetry. In both CP and HS, the incidence of large slow waves within individual NREM epochs tended to differ across hemispheres, with a relative overall predominance of the right over the left hemisphere. The absolute magnitude of this asymmetry was greater in CP relative to HS. However, the CC resection had no significant effects on the distribution of slow wave origin probability across hemispheres. Present results indicate that CC integrity is essential for the cross-hemispheric traveling of human sleep slow waves, in line with the assumption of a direct relationship between white matter integrity and slow wave propagation. Our findings also revealed a residual cross-hemispheric slow wave propagation that may rely on alternative pathways, including cortico-subcortico-cortical loops. Finally, this data indicate that the lack of the CC does not lead to differences in slow wave generation across brain hemispheres.

Significance Statement
The slow waves of NREM-sleep behave as traveling waves and their propagation has been suggested to reflect the integrity of white matter cortico-cortical connections. To directly assess this hypothesis, here we investigated the role of the corpus callosum in the cortical spreading of NREM slow waves through the study of a rare population of totally callosotomized patients. Our results demonstrate a causal role of the corpus callosum in the cross-hemispheric traveling of sleep slow waves. Additionally, we found that callosotomy does not affect the relative tendency of each hemisphere at generating slow waves. Incidentally, we also found that slow waves tend to originate more often in the right than in the left hemisphere in both callosotomized and healthy adult individuals.
Original languageEnglish
Pages (from-to)5589-5603
Number of pages15
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume40
Issue number29
Early online date15 Jun 2020
DOIs
Publication statusPublished - 15 Jul 2020

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