Fear‐containing dreams serve an emotion regulation function; the stronger the recruitment of fear‐responsive regions during dreaming, the weaker their response to actual fear‐eliciting stimuli during wakefulness

Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis. Virginie Sterpenich et al. Human Brain Mapping, October 30 2019. https://doi.org/10.1002/hbm.24843

Abstract: Recent neuroscientific theories have proposed that emotions experienced in dreams contribute to the resolution of emotional distress and preparation for future affective reactions. We addressed one emerging prediction, namely that experiencing fear in dreams is associated with more adapted responses to threatening signals during wakefulness. Using a stepwise approach across two studies, we identified brain regions activated when experiencing fear in dreams and showed that frightening dreams modulated the response of these same regions to threatening stimuli during wakefulness. Specifically, in Study 1, we performed serial awakenings in 18 participants recorded throughout the night with high‐density electroencephalography (EEG) and asked them whether they experienced any fear in their dreams. Insula and midcingulate cortex activity increased for dreams containing fear. In Study 2, we tested 89 participants and found that those reporting higher incidence of fear in their dreams showed reduced emotional arousal and fMRI response to fear‐eliciting stimuli in the insula, amygdala and midcingulate cortex, while awake. Consistent with better emotion regulation processes, the same participants displayed increased medial prefrontal cortex activity. These findings support that emotions in dreams and wakefulness engage similar neural substrates, and substantiate a link between emotional processes occurring during sleep and emotional brain functions during wakefulness.

1 INTRODUCTION

Converging evidence from human and animal research suggests functional links between sleep and emotional processes (Boyce, Glasgow, Williams, & Adamantidis, 2016; Perogamvros & Schwartz, 2012; Wagner, Hallschmid, Rasch, & Born, 2006; Walker & van der Helm, 2009). Chronic sleep disruption can lead to increased aggressiveness (Kamphuis, Meerlo, Koolhaas, & Lancel, 2012) and negative mood states (Zohar, Tzischinsky, Epstein, & Lavie, 2005), whereas affective disorders such as depression and post‐traumatic stress disorder (PTSD) are frequently associated with sleep abnormalities (e.g., insomnia and nightmares). Experimental evidence indicates that acute sleep deprivation impairs the prefrontal control over limbic regions during wakefulness, hence, exacerbating emotional responses to negative stimuli (Yoo, Gujar, Hu, Jolesz, & Walker, 2007). Neuroimaging and intracranial data further established that, during human sleep, emotional limbic networks are activated (e.g., Braun et al., 1997; Corsi‐Cabrera et al., 2016; Maquet et al., 1996; Nofzinger, Mintun, Wiseman, Kupfer, & Moore, 1997; Schabus et al., 2007). Together these findings indicate that sleep physiology may offer a permissive condition for affective information to be reprocessed and reorganized. Yet, it remains unsettled whether such emotion regulation processes also happen at the subjective, experiential level during sleep, and may be expressed in dreams. Several influential theoretical models formalized this idea. For example, the threat simulation theory postulated that dreaming may fulfill a neurobiological function by allowing an offline simulation of threatening events and rehearsal of threat‐avoidance skills, through the activation of a fear‐related amygdalocortical network (Revonsuo, 2000; Valli et al., 2005). Such mechanism would promote adapted behavioral responses in real life situations (Valli & Revonsuo, 2009). By contrast, other models suggested that dreaming would facilitate the resolution of current emotional conflict (Cartwright, Agargun, Kirkby, & Friedman, 2006; Cartwright, Luten, Young, Mercer, & Bears, 1998), the reduction of next‐day negative mood (Schredl, 2010) and extinction learning (Nielsen & Levin, 2007). Although these two main theoretical lines differ, because one focuses on the optimization of waking affective reactions (Perogamvros & Schwartz, 2012; Revonsuo, 2000) and the other on the resolution of current emotional distress (e.g., fear extinction; Nielsen & Levin, 2007), both converge to suggest that experiencing fear in dreams leads to more adapted responses to threatening signals during wakefulness (Scarpelli, Bartolacci, D'Atri, Gorgoni, & De Gennaro, 2019). The proposed mechanism is that memories from a person's affective history are replayed in the virtual and safe environment of the dream so that they can be reorganized (Nielsen & Levin, 2007; Perogamvros & Schwartz, 2012). From a neuroscience perspective, one key premise of these theoretical models is that experiencing emotions in dreams implicates the same brain circuits as in wakefulness (Hobson & Pace‐Schott, 2002; Schwartz, 2003). Preliminary evidence from two anatomical investigations showed that impaired structural integrity of the left amygdala was associated with reduced emotional intensity in dreams (Blake, Terburg, Balchin, van Honk, & Solms, 2019; De Gennaro et al., 2011).

Like during wakefulness, people experience a large variety of emotions in their dreams, with rapid eye movement (REM) dreaming being usually more emotionally loaded than non‐rapid eye movement (NREM) dreams (Carr & Nielsen, 2015; Smith et al., 2004). While some studies found a relative predominance of negative emotions, such as fear and anxiety, in dreams (Merritt, Stickgold, Pace‐Schott, Williams, & Hobson, 1994; Roussy et al., 2000), others reported a balance of positive and negative emotions (Schredl & Doll, 1998), or found that joy and emotions related to approach behaviors may prevail (Fosse, Stickgold, & Hobson, 2001; Malcolm‐Smith, Koopowitz, Pantelis, & Solms, 2012). When performing a lexicostatistical analysis of large data sets of dream reports, a clear dissociation between dreams containing basic, mostly fear‐related, emotions and those with other more social emotions (e.g., embarrassment, excitement, frustration) was found, highlighting distinct affective modes operating during dreaming, with fear in dreams representing a prevalent and biologically‐relevant emotional category (Revonsuo, 2000; Schwartz, 2004). Thus, if fear‐containing dreams serve an emotion regulation function, as hypothesized by the theoretical models, the stronger the recruitment of fear‐responsive brain regions (e.g., amygdala, cingulate cortex, and insula; see Phan, Wager, Taylor, & Liberzon, 2002) during dreaming, the weaker the response of these same regions to actual fear‐eliciting stimuli during wakefulness should be. This compensatory or homeostatic mechanism may also be accompanied by an enhanced recruitment of emotion regulation brain regions (such as the medial prefrontal cortex, mPFC, which is implicated in fear extinction) during wakefulness (Dunsmoor et al., 2019; Phelps, Delgado, Nearing, & LeDoux, 2004; Quirk, Likhtik, Pelletier, & Pare, 2003; Yoo et al., 2007).

Here, we collected dream reports and functional brain measures using high‐density EEG (hdEEG) and functional MRI (fMRI) across two studies to address the following questions: (a) do emotions in dreams (here fear‐related emotions) engage the same neural circuits as during wakefulness and (b) is there a link between emotions experienced in dreams and brain responses to emotional stimuli during wakefulness. By addressing these fundamental and complementary topics, we aim at clarifying the grounding conditions for the study of dreaming as pertaining to day/night affective homeostasis.