TY - JOUR
T1 - Losing neutrality
T2 - The neural basis of impaired emotional control without sleep
AU - Simon, Eti Ben
AU - Oren, Noga
AU - Sharon, Haggai
AU - Kirschner, Adi
AU - Goldway, Noam
AU - Okon-Singer, Hadas
AU - Tauman, Rivi
AU - Deweese, Menton M.
AU - Keil, Andreas
AU - Hendler, Talma
N1 - Publisher Copyright:
© 2015 the authors.
PY - 2015/9/23
Y1 - 2015/9/23
N2 - 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.
AB - 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.
KW - Amygdala
KW - Cognitive-emotional interactions
KW - Emotion
KW - FMRI
KW - Sleep deprivation
KW - SsVEP
UR - http://www.scopus.com/inward/record.url?scp=84942134945&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.1314-15.2015
DO - 10.1523/JNEUROSCI.1314-15.2015
M3 - Article
C2 - 26400948
AN - SCOPUS:84942134945
SN - 0270-6474
VL - 35
SP - 13194
EP - 13205
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 38
ER -