title: Losing Neutrality: The Neural Basis of Impaired Emotional Control without Sleep.
abstract: Sleep deprivation has been shown recently to alter emotional processing possibly associated with reduced frontal regulation. Such impairments can ultimately fail adaptive attempts to regulate emotional processing (also known as cognitive control of emotion), although this hypothesis has not been examined directly. Therefore, we explored the influence of sleep deprivation on the human brain using two different cognitive-emotional tasks, recorded using fMRI and EEG. Both tasks involved irrelevant emotional and neutral distractors presented during a competing cognitive challenge, thus creating a continuous demand for regulating emotional processing. Results reveal that, although participants showed enhanced limbic and electrophysiological reactions to emotional distractors regardless of their sleep state, they were specifically unable to ignore neutral distracting information after sleep deprivation. As a consequence, sleep deprivation resulted in similar processing of neutral and negative distractors, thus disabling accurate emotional discrimination. As expected, these findings were further associated with a decrease in prefrontal connectivity patterns in both EEG and fMRI signals, reflecting a profound decline in cognitive control of emotion. Notably, such a decline was associated with lower REM sleep amounts, supporting a role for REM sleep in overnight emotional processing. Altogether, our findings suggest that losing sleep alters emotional reactivity by lowering the threshold for emotional activation, leading to a maladaptive loss of emotional neutrality. Significance statement: Sleep loss is known as a robust modulator of emotional reactivity, leading to increased anxiety and stress elicited by seemingly minor triggers. In this work, we aimed to portray the neural basis of these emotional impairments and their possible association with frontal regulation of emotional processing, also known as cognitive control of emotion. Using specifically suited EEG and fMRI tasks, we were able to show that sleep deprivation alters emotional reactivity by triggering enhanced processing of stimuli regarded previously as neutral. These changes were further accompanied by diminished frontal connectivity, reduced REM sleep, and poorer performance. Therefore, we suggest that sleep loss alters emotional reactivity by lowering the threshold for emotional activation, leading to a maladaptive loss of emotional neutrality.
authors.affiliation: Functional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Medical Center, Tel Aviv 6423906, Israel, Sackler Faculty of Medicine and etoosh@gmail.com talma@tasmc.health.gov.il.
authors.forename: Eti Ben
authors.identifier: http://orcid.org/0000-0002-3862-8288
authors.initials: EB
authors.lastname: Simon
authors.affiliation: Functional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Medical Center, Tel Aviv 6423906, Israel, Sackler Faculty of Medicine and.
authors.forename: Noga
authors.initials: N
authors.lastname: Oren
authors.affiliation: Functional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Medical Center, Tel Aviv 6423906, Israel, Sackler Faculty of Medicine and.
authors.forename: Haggai
authors.identifier: http://orcid.org/0000-0003-1981-658X
authors.initials: H
authors.lastname: Sharon
authors.affiliation: Sagol School of Neuroscience and.
authors.forename: Adi
authors.initials: A
authors.lastname: Kirschner
authors.affiliation: Sagol School of Neuroscience and.
authors.forename: Noam
authors.initials: N
authors.lastname: Goldway
authors.affiliation: Department of Psychology, University of Haifa, Haifa 3498838, Israel.
authors.forename: Hadas
authors.initials: H
authors.lastname: Okon-Singer
authors.affiliation: Sackler Faculty of Medicine and Sleep Disorders Center, Tel Aviv Medical Center, Tel Aviv 6330303, Israel, and.
authors.forename: Rivi
authors.initials: R
authors.lastname: Tauman
authors.affiliation: Center for the Study of Emotion and Attention, University of Florida, Gainesville, Florida 32611.
authors.forename: Menton M
authors.initials: MM
authors.lastname: Deweese
authors.affiliation: Center for the Study of Emotion and Attention, University of Florida, Gainesville, Florida 32611.
authors.forename: Andreas
authors.initials: A
authors.lastname: Keil
authors.affiliation: Functional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Medical Center, Tel Aviv 6423906, Israel, Sackler Faculty of Medicine and Sagol School of Neuroscience and School of Psychological Sciences, Tel Aviv University, Tel Aviv 6997801, Israel, etoosh@gmail.com talma@tasmc.health.gov.il.
authors.forename: Talma
authors.initials: T
authors.lastname: Hendler
mesh_terms: D000328:Adult; D000704:Analysis of Variance; D001921:Brain / Q000098:blood supply / Q000503:physiopathology*; D001931:Brain Mapping; D004569:Electroencephalography; D005074:Evoked Potentials, Visual / Q000502:physiology*; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D019964:Mood Disorders / Q000209:etiology* / Q000473:pathology*; D010100:Oxygen / Q000097:blood; D010775:Photic Stimulation; D011930:Reaction Time; D012892:Sleep Deprivation / Q000150:complications*; D055815:Young Adult
chemical_list: D010100:Oxygen
keywords: amygdala; cognitive-emotional interactions; emotion; fMRI; sleep deprivation; ssVEP