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.

The sleep-deprived human brain

“…Consistent with the failure to accurately code positive, reward incentive signals (described above), one night of SD impairs the discrimination of faces expressing negative emotions by viscerosensory regions of the anterior insula and anterior cingulate cortices, and to a degree, the subcortical amygdala 95 . Similarly, sleep loss results in generalized, nonspecific increases in amygdala activity (as measured by fMRI or electroencephalography) in response to aversive and neutral emotional pictures 96,97 .…”

The key role of insomnia and sleep loss in the dysregulation of multiple systems involved in mood disorders: A proposed model

“…Insomnia and sleep loss have been proposed to lead to maladaptive emotional regulation, and consequently to exaggerated neural and behavioural reactivity to experiences and reward (Altena et al, 2016;Baglioni et al, 2010;Boudebesse & Henry, 2012;Gujar et al, 2011;Krause et al, 2017;McKenna & Eyler, 2012;Yoo, Gujar, Hu, Jolesz, & Walker, 2007). In addition, they are related to impairments in basic cognitive functions and higher-order cognitive processing of executive functions involved in supervisory control, problem-solving, flexibility, self-control and decision-making (Killgore, 2010;Krause et al, 2017;Ma, Dinges, Basner, & Rao, 2015;Pilcher, Morris, Donnelly, & Feigl, 2015;Raven et al, 2017;Rossa, Smith, Allan, & Sullivan, 2014;Simon et al, 2015;Venkatraman, Chuah, Huettel, & Chee, 2007), as well as to impulsive and aggressive behaviours (Acheson, Richards, & de Wit, 2007;Kamphuis et al, 2014;Rossa et al, 2014) and, consequently, to the increased risk of suicidality (for an overview, see Woznica et al, 2015). At the neural level, neuroimaging studies have revealed that emotional and reward networks are activated during sleep.…”

Shortened sleep fuels inflammatory responses to marital conflict: Emotion regulation matters

“…On the one hand, short sleep may increase both inflammation and interpersonal conflict by disrupting emotion regulation. For instance, total sleep deprivation reduced neural communication between emotion-relevant brain regions, resulting in poorer discrimination of emotion cues (Simon et al, 2015; Yoo et al, 2007). Emotion expression may also suffer with shortened sleep: following sleep deprivation, people were less facially expressive and used more negative emotion words and fewer positive words than after a full night of sleep (McGlinchey, 2011; Minkel et al, 2011).…”