Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala
Emotional memories are preferentially consolidated during sleep, through the process of memory reactivation. Targeted memory reactivation (TMR) has been shown to boost memory consolidation during sleep, but its neural correlates remain unclear, particularly for emotional memories. Here, we aimed to...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-06-01
|
| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922002488 |
| _version_ | 1818772769780793344 |
|---|---|
| author | Sofia Isabel Ribeiro Pereira Maria-Efstratia Tsimpanouli Isabel Hutchison Jules Schneider Ian M. Anderson Martyn McFarquhar Rebecca Elliott Penelope A. Lewis |
| author_facet | Sofia Isabel Ribeiro Pereira Maria-Efstratia Tsimpanouli Isabel Hutchison Jules Schneider Ian M. Anderson Martyn McFarquhar Rebecca Elliott Penelope A. Lewis |
| author_sort | Sofia Isabel Ribeiro Pereira |
| collection | DOAJ |
| description | Emotional memories are preferentially consolidated during sleep, through the process of memory reactivation. Targeted memory reactivation (TMR) has been shown to boost memory consolidation during sleep, but its neural correlates remain unclear, particularly for emotional memories. Here, we aimed to examine how TMR of emotional material during slow wave sleep (SWS) impacts upon neural processing during a subsequent arousal rating task. Participants were trained on a spatial memory task including negative and neutral pictures paired with semantically matching sounds. The picture-sound pairs were rated for emotional arousal before and after the spatial memory task. Then, half of the sounds from each emotional category (negative and neutral) were cued during SWS. The next day, participants were retested on both the arousal rating and the spatial memory task inside an MRI scanner, followed by another retest session a week later. Memory consolidation and arousal processing did not differ between cued and non-cued items of either emotional category. We found increased responses to emotional stimuli in the amygdala and orbitofrontal cortex (OFC), and a cueing versus emotion interaction in the OFC, whereby cueing neutral stimuli led to an increase in OFC activity, while cueing negative stimuli led to decreased OFC activation. Interestingly, the effect of cueing on amygdala activation was modulated by time spent in REM sleep. We conclude that SWS TMR impacts OFC activity, while REM sleep plays a role in mediating the effect of such cueing on amygdala. |
| first_indexed | 2024-12-18T10:14:37Z |
| format | Article |
| id | doaj.art-042a0f70c0284c48b6684a88354b90c3 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-18T10:14:37Z |
| publishDate | 2022-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-042a0f70c0284c48b6684a88354b90c32022-12-21T21:11:20ZengElsevierNeuroImage1095-95722022-06-01253119120Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdalaSofia Isabel Ribeiro Pereira0Maria-Efstratia Tsimpanouli1Isabel Hutchison2Jules Schneider3Ian M. Anderson4Martyn McFarquhar5Rebecca Elliott6Penelope A. Lewis7School of Psychology, Cardiff University Brain Research Imaging Centre, Cardiff, Wales, CF24 4HQ, UK; Corresponding authors.School of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychology, Cardiff University Brain Research Imaging Centre, Cardiff, Wales, CF24 4HQ, UK; School of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UKSchool of Psychology, Cardiff University Brain Research Imaging Centre, Cardiff, Wales, CF24 4HQ, UK; School of Psychological Sciences, University of Manchester, Manchester, M13 9PL, UK; Corresponding authors.Emotional memories are preferentially consolidated during sleep, through the process of memory reactivation. Targeted memory reactivation (TMR) has been shown to boost memory consolidation during sleep, but its neural correlates remain unclear, particularly for emotional memories. Here, we aimed to examine how TMR of emotional material during slow wave sleep (SWS) impacts upon neural processing during a subsequent arousal rating task. Participants were trained on a spatial memory task including negative and neutral pictures paired with semantically matching sounds. The picture-sound pairs were rated for emotional arousal before and after the spatial memory task. Then, half of the sounds from each emotional category (negative and neutral) were cued during SWS. The next day, participants were retested on both the arousal rating and the spatial memory task inside an MRI scanner, followed by another retest session a week later. Memory consolidation and arousal processing did not differ between cued and non-cued items of either emotional category. We found increased responses to emotional stimuli in the amygdala and orbitofrontal cortex (OFC), and a cueing versus emotion interaction in the OFC, whereby cueing neutral stimuli led to an increase in OFC activity, while cueing negative stimuli led to decreased OFC activation. Interestingly, the effect of cueing on amygdala activation was modulated by time spent in REM sleep. We conclude that SWS TMR impacts OFC activity, while REM sleep plays a role in mediating the effect of such cueing on amygdala.http://www.sciencedirect.com/science/article/pii/S1053811922002488SleepTargeted memory reactivationEmotional memorySwsSpatial memory taskArousal |
| spellingShingle | Sofia Isabel Ribeiro Pereira Maria-Efstratia Tsimpanouli Isabel Hutchison Jules Schneider Ian M. Anderson Martyn McFarquhar Rebecca Elliott Penelope A. Lewis Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala NeuroImage Sleep Targeted memory reactivation Emotional memory Sws Spatial memory task Arousal |
| title | Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala |
| title_full | Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala |
| title_fullStr | Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala |
| title_full_unstemmed | Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala |
| title_short | Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala |
| title_sort | cueing emotional memories during slow wave sleep modulates next day activity in the orbitofrontal cortex and the amygdala |
| topic | Sleep Targeted memory reactivation Emotional memory Sws Spatial memory task Arousal |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922002488 |
| work_keys_str_mv | AT sofiaisabelribeiropereira cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT mariaefstratiatsimpanouli cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT isabelhutchison cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT julesschneider cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT ianmanderson cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT martynmcfarquhar cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT rebeccaelliott cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala AT penelopealewis cueingemotionalmemoriesduringslowwavesleepmodulatesnextdayactivityintheorbitofrontalcortexandtheamygdala |