title: Neural and behavioral correlates of extended training during sleep deprivation in humans: evidence for local, task-specific effects.
abstract: Recent work has demonstrated that behavioral manipulations targeting specific cortical areas during prolonged wakefulness lead to a region-specific homeostatic increase in theta activity (5-9 Hz), suggesting that theta waves could represent transient neuronal OFF periods (local sleep). In awake rats, the occurrence of an OFF period in a brain area relevant for behavior results in performance errors. Here we investigated the potential relationship between local sleep events and negative behavioral outcomes in humans. Volunteers participated in two prolonged wakefulness experiments (24 h), each including 12 h of practice with either a driving simulation (DS) game or a battery of tasks based on executive functions (EFs). Multiple high-density EEG recordings were obtained during each experiment, both in quiet rest conditions and during execution of two behavioral tests, a response inhibition test and a motor test, aimed at assessing changes in impulse control and visuomotor performance, respectively. In addition, fMRI examinations obtained at 12 h intervals were used to investigate changes in inter-regional connectivity. The EF experiment was associated with a reduced efficiency in impulse control, whereas DS led to a relative impairment in visuomotor control. A specific spatial and temporal correlation was observed between EEG theta waves occurring in task-related areas and deterioration of behavioral performance. The fMRI connectivity analysis indicated that performance impairment might partially depend on a breakdown in connectivity determined by a "network overload." Present results demonstrate the existence of an association between theta waves during wakefulness and performance errors and may contribute explaining behavioral impairments under conditions of sleep deprivation/restriction.
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519, Laboratory of Clinical Biochemistry and Molecular Biology, and Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, 56126 Pisa, Italy, and.
authors: Giulio
authors: http://orcid.org/0000-0003-4045-7075
authors: G
authors: Bernardi
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519.
authors: Francesca
authors: F
authors: Siclari
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519.
authors: Xiaoqian
authors: X
authors: Yu
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519.
authors: Corinna
authors: C
authors: Zennig
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519.
authors: Michele
authors: M
authors: Bellesi
authors: Laboratory of Clinical Biochemistry and Molecular Biology, and Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, 56126 Pisa, Italy, and.
authors: Emiliano
authors: http://orcid.org/0000-0002-7178-9534
authors: E
authors: Ricciardi
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519.
authors: Chiara
authors: http://orcid.org/0000-0003-2563-677X
authors: C
authors: Cirelli
authors: Department of Physiology and Pharmacology, City University of New York Medical School, New York, New York 10017.
authors: Maria Felice
authors: MF
authors: Ghilardi
authors: Laboratory of Clinical Biochemistry and Molecular Biology, and Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, 56126 Pisa, Italy, and pietro.pietrini@med.unipi.it gtononi@wisc.edu.
authors: Pietro
authors: P
authors: Pietrini
authors: Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53519, pietro.pietrini@med.unipi.it gtononi@wisc.edu.
authors: Giulio
authors: G
authors: Tononi
mesh_terms: D000328:Adult; D001921:Brain / Q000502:physiology*; D004569:Electroencephalography / Q000379:methods; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging / Q000379:methods; D008297:Male; D009415:Nerve Net / Q000502:physiology*; D010775:Photic Stimulation / Q000379:methods; D011597:Psychomotor Performance / Q000502:physiology*; D012146:Rest / Q000502:physiology / Q000523:psychology; D012892:Sleep Deprivation / Q000175:diagnosis* / Q000523:psychology; D013826:Theta Rhythm / Q000502:physiology*; D014851:Wakefulness / Q000502:physiology*; D055815:Young Adult
keywords: fMRI; hd-EEG; impulse control; local sleep; performance; theta waves