Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Sterpenich, Virginie; Piguet, Camille; Desseilles, Martin; Ceravolo, Léonardo; Gschwind, Markus; Ville, Dimitri Van De; Vuilleumier, Patrik; Schwartz, Sophie

doi:10.1016/j.neuroimage.2014.06.003

“…All participants filled out the same questionnaires on sleep quality (PSQI, Tzourio-Mazoyer N et al 2002), daytime sleepiness (Epworth sleepiness scale, ESS, Pascual-Marqui RD 2002), depression (Beck Depression Scale, BDI, Mensen A and R Khatami 2013), anxiety (State-Trait Anxiety Inventory Trait, STAI-T, Spielberger CD et al 1970), and also kept the same sleep and dream diary. These results correspond to a secondary analysis because part of the data was already presented elsewhere (Sterpenich V, C Piguet, et al 2014;Sterpenich V et al 2017), yet without exploring any of the dream measurements. Note that the sleep and dream diaries were designed specifically for this analysis and the stimuli of the three different studies correspond to similar visual items (emotional and neutral pictures, see below), eliciting similar changes in emotional arousal and in local brain activition ( Fig.…”

Section: Study 2: Modulation Of Brain Responses To Aversive Stimuli Dsupporting

confidence: 75%

“…Data from three different fMRI experiments were included in the analysis. Two of these three sets of data have already been reported elsewhere, but none of these former publications concerned emotions in dreams (Sterpenich V, C Piguet, et al 2014;Sterpenich V et al 2017). Common to these three experiments was that participants were exposed to aversive and neutral images, and that dream data were collected using the exact same instructions and dream diary.…”

Section: Emotional Tasksmentioning

confidence: 99%

“…In Experiment 1, participants were presented with conditioned (aversive) and unconditioned faces. Stimuli were presented in an intermixed, random order, one at a time (2.5 s each) followed by a varying interval (ISI: 4-5.5 s, mean=4.75) (see Sterpenich V, C Piguet, et al 2014 for more details). In Experiment 2, 60 aversive, 60 funny and 60 neutral pictures were presented to participants.…”

Section: Emotional Tasksmentioning

confidence: 99%

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Fear in dreams and in wakefulness: evidence for day/night affective homeostasis

Sterpenich

¹

,

Perogamvros

²

,

Tononi

³

et al. 2019

Preprint

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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 highdensity 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. SIGNIFICANT STATEMENTHighly debated while pivotal to current theoretical models of dreaming, the relationship between emotion processing during wakefulness and in dreams remains elusive. In a first study, we used high-density EEG recordings and observed that regions involved in fear processing (i.e. the insula and midcingulate cortex) were activated during fear-related dreams. This first finding demonstrates that emotions in dreams engage similar neural circuits as during wakefulness. In a second study, using fMRI, we show that higher incidence of fear in dreams was associated with reduced emotional arousal and brain responses indicative of better emotion regulation during wakefulness. Together, these results strongly support the idea that experiencing fear in a secure environment, as in dreams, relates to more adapted responses to threatening events in real life. 2000), others reported a balance of positive and negative emotions (Schredl M and E Doll 1998), or found that joy and emotions related to approach behaviors may prevail (Fosse R et al. 2001;Malcolm-Smith S et al. 2012). When performing a lexicostatistical analysis of large datasets 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 A 2000;Schwartz S 2004). Thus, if fear-containing dreams serve an emotion regulation f...

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“…All participants filled out the same questionnaires on sleep quality (PSQI, Buysse, et al, ), daytime sleepiness (Epworth sleepiness scale, ESS, Johns, ), depression (beck depression scale, BDI, Beck, Steer, & Brown, ), anxiety (state–trait anxiety inventory trait, STAI‐T, Spielberger, Gorsuch, & Lushene, ), and also kept the same sleep and dream diary. Study 2 correspond to a secondary analysis because part of the data was already presented elsewhere (Sterpenich et al, ; Sterpenich, Ceravolo, & Schwartz, ), yet without exploring any of the dream measurements. Note that the sleep and dream diaries were designed specifically for this analysis and the stimuli of the three different studies correspond to similar visual items (emotional and neutral pictures, see below), eliciting similar changes in emotional arousal and in local brain activation (Figure S1).…”

Section: Methodsmentioning

confidence: 99%

Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis

Sterpenich

¹

,

Perogamvros

²

,

Tononi

³

et al. 2019

Human Brain Mapping

Self Cite

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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.

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“…1E), pairing the target tone with NB stimulation improved discrimination among similar tones (Froemke et al 2013). After visually cued discriminative aversive conditioning in humans, images of faces that had been paired with an aversive white noise burst were more effectively recognized after being morphed with distractors than faces that had not, though this effect required a period of sleep in between training and testing (Sterpenich et al 2014). However, in rats, simple conditioning that used a single odor during fear conditioning was found to broaden olfactory tuning curves in the piriform cortex, consistent with generalization rather than discrimination, while discriminative conditioning using multiple odors instead narrowed tuning curves, suggesting enhanced discrimination (Chen et al 2011).…”

Section: Sensory Functionsmentioning

confidence: 96%

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

McGann

¹

2015

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Historically, the body's sensory systems have been presumed to provide the brain with raw information about the external environment, which the brain must interpret to select a behavioral response. Consequently, studies of the neurobiology of learning and memory have focused on circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus-specific changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. This review synthesizes evidence across sensory modalities to report emerging themes, including the systems' flexibility to emphasize different aspects of a sensory stimulus depending on its predictive features and ability of different forms of learning to produce similar plasticity in sensory structures. Potential functions of this learning-induced neuroplasticity are discussed in relation to the challenges faced by sensory systems in changing environments, and evidence for absolute changes in sensory ability is considered. We also emphasize that this plasticity may serve important nonsensory functions, including balancing metabolic load, regulating attentional focus, and facilitating downstream neuroplasticity.

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Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Cited by 17 publications

References 59 publications

Fear in dreams and in wakefulness: evidence for day/night affective homeostasis

Fear in dreams and in wakefulness: evidence for day/night affective homeostasis

Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

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