Focal lesions induce large-scale percolation of sleep-like intracerebral activity in awake humans
S. Russo,
A. Pigorini,
E. Mikulan,
S. Sarasso,
A. Rubino,
F.M. Zauli,
S. Parmigiani,
P. d'Orio,
A. Cattani,
S. Francione,
L. Tassi,
C.L.A. Bassetti,
G. Lo Russo,
L. Nobili,
I. Sartori,
M. Massimini
Affiliations
S. Russo
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
A. Pigorini
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
E. Mikulan
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
S. Sarasso
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
A. Rubino
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
F.M. Zauli
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
S. Parmigiani
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy
P. d'Orio
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy; Institute of Neuroscience, CNR, via Volturno 39E, 43125 Parma, Italy
A. Cattani
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy; Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, 53719, USA
S. Francione
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
L. Tassi
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
C.L.A. Bassetti
Department of Neurology, Inselspital, University of Bern, Switzerland
G. Lo Russo
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
L. Nobili
Child Neuropsychiatry, IRCCS Istituto G. Gaslini, Genova 16147, Italy; Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DiNOGMI), University of Genoa, Genoa, Italy
I. Sartori
''C. Munari'' Epilepsy Surgery Centre, Department of Neuroscience, Niguarda Hospital, Milan 20162, Italy
M. Massimini
Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy; IRCCS, Fondazione Don Carlo Gnocchi, Milan 20148, Italy; Azrieli Program in Brain, Mind and Consciousness, Canadian Institute for Advanced Research, Toronto, Canada; Corresponding author at: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, Italy.
Focal cortical lesions are known to result in large-scale functional alterations involving distant areas; however, little is known about the electrophysiological mechanisms underlying these network effects. Here, we addressed this issue by analysing the short and long distance intracranial effects of controlled structural lesions in humans. The changes in Stereo-Electroencephalographic (SEEG) activity after Radiofrequency-Thermocoagulation (RFTC) recorded in 21 epileptic subjects were assessed with respect to baseline resting wakefulness and sleep activity. In addition, Cortico-Cortical Evoked Potentials (CCEPs) recorded before the lesion were employed to interpret these changes with respect to individual long-range connectivity patterns. We found that small structural ablations lead to the generation and large-scale propagation of sleep-like slow waves within the awake brain. These slow waves match those recorded in the same subjects during sleep, are prevalent in perilesional areas, but can percolate up to distances of 60 mm through specific long-range connections, as predicted by CCEPs. Given the known impact of slow waves on information processing and cortical plasticity, demonstrating their intrusion and percolation within the awake brain add key elements to our understanding of network dysfunction after cortical injuries.
