Advertisement

Brain Topography

, Volume 30, Issue 5, pp 629–638 | Cite as

Predicting Dream Recall: EEG Activation During NREM Sleep or Shared Mechanisms with Wakefulness?

  • Serena Scarpelli
  • Aurora D’Atri
  • Anastasia Mangiaruga
  • Cristina Marzano
  • Maurizio Gorgoni
  • Cinzia Schiappa
  • Michele Ferrara
  • Luigi De GennaroEmail author
Original Paper

Abstract

The common knowledge of a uniqueness of REM sleep as a privileged scenario of dreaming still persists, although consolidated empirical evidence shows that the assumption that dreaming is just an epiphenomenon of REM sleep is no longer tenable. However, the brain mechanisms underlying dream generation and its encoding in memory during NREM sleep are still mostly unknown. In fact, only few studies have investigated on the mechanisms of dream phenomenology related to NREM sleep. For this reason, our study is specifically aimed to elucidate the electrophysiological (EEG) correlates of dream recall (DR) upon NREM sleep awakenings. Under the assumption that EEG activity predicts the presence/absence of DR also during NREM sleep, we have investigated whether DR from stage 2 NREM sleep shares similar brain mechanisms to those involved in the encoding of episodic memory during wakefulness, or it depends on the specific electrophysiological milieu of the sleep period along the desynchronized/synchronized EEG continuum. We collected DR from a multiple nap protocol in a within-subjects design. We found that DR is predicted by an extensive reduction of delta activity during the last segment of sleep, encompassing left frontal and temporo-parietal areas. The results could represent an update on the mechanisms underlying the sleep mentation during NREM sleep. In particular, they support the hypothesis that an increased cortical EEG activation is a prerequisite for DR, and they are not necessarily in conflict with the hypothesis of common wake-sleep mechanisms. We also confirmed that EEG correlates of DR depend on a state-like relationship.

Keywords

Dream recall EEG correlates NREM sleep Nap Activation model Delta activity 

Notes

Acknowledgements

This work was supported by a grant to Luigi De Gennaro from “Progetti di Ricerca di Ateneo 2014 (C26A143ZEP), 2015 (C26A158K25)” (“Sapienza” University of Rome).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all subjects after the nature and possible consequences of the studies were explained.

References

  1. Addante RJ, Watrous AJ, Yonelinas AP, Ekstrom AD, Ranganath C (2011) Prestimulus theta activity predicts correct source memory retrieval. Proc Natl Acad Sci USA 108:10702–10707. doi: 10.1073/pnas.1014528108 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antrobus JS (1987) Cortical hemisphere asymmetry and sleep mentation. Psychol Rev 94:359–368. doi: 10.1037/0033-295X.98.1.96 CrossRefPubMedGoogle Scholar
  3. Antrobus JS (1991) Dreaming: cognitive processes during cortical activation and high afferent thresholds. Psychol Rev 98:96–121. doi: 10.1037/0033-295X.94.3.359 CrossRefPubMedGoogle Scholar
  4. Bernardi G, Siclari F, Yu X, Zennig C, Bellesi M, Ricciardi E, Cirelli C, Ghilardi MF, Pietrini P, Tononi G (2015) Neural and behavioral correlates of extended training during sleep deprivation in humans: evidence for local, task-specific effects. J Neurosci 35:4487–4500. doi: 10.1523/JNEUROSCI.4567-14.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Caplan JB, Kahana MJ, Raghavachari S, Madsen JR (2001) Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. J Neurophysiol 86:368–380PubMedGoogle Scholar
  6. Carrasco E, Santamaria J, Iranzo A, Pintor L, Pablo JD, Solanas A, Kumru H, Martìnez-Rodrìguez JE, Boget T (2006) Changes in dreaming induced by CPAP in severe obstructive sleep apnea syndrome patients. J Sleep Res 15:430–436. doi: 10.1111/j.1365-2869.2006.00553.x CrossRefPubMedGoogle Scholar
  7. Charney DS, Soldatos CR, Bixler EO, Kales A (1977) Factors contributing to dream recall in insomniac subjects. Sleep Res 6:126Google Scholar
  8. Chellappa SL, Frey S, Knoblauch V, Cajochen C (2011) Cortical activation patterns herald successful dream recall after NREM and REM sleep. Biol Psychol 87:251–256. doi: 10.1016/j.biopsycho.2011.03.004 CrossRefPubMedGoogle Scholar
  9. Cipolli C, Ferrara M, De Gennaro L, Plazzi G (2016) Beyond the neuropsychology of dreaming: Insights into the neural basis of dreaming with new techniques of sleep recording and analysis. Sleep Med Rev. doi: 10.1016/j.smrv.2016.07.005 PubMedGoogle Scholar
  10. Curcio G, Tempesta D, Scarlata S, Marzano C, Moroni F, Rossini PM, Ferrara M, De Gennaro L (2013) Validity of the Italian version of the Pittsburgh sleep quality index (PSQI). Neurol Sci 34:511–519. doi: 10.1007/s10072-012-1085-y CrossRefPubMedGoogle Scholar
  11. De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7:423–440. doi: 10.1053/smrv.2002.0252 CrossRefPubMedGoogle Scholar
  12. De Gennaro L, Marzano C, Moroni F, Curcio G, Ferrara M, Cipolli C (2010) Recovery sleep after sleep deprivation almost completely abolishes dream recall. Behav Brain Res 206:293–298. doi: 10.1016/j.bbr.2009.09.030 CrossRefPubMedGoogle Scholar
  13. De Gennaro L, Cipolli C, Cherubini A, Assogna F, Cacciari C, Marzano C, Curcio G, Ferrara M, Caltagirone C, Spalletta G (2011) Amygdala and hippocampus volumetry and diffusivity in relation to dreaming. Hum Brain Map 32:1458–1470. doi: 10.1002/hbm.21120 CrossRefGoogle Scholar
  14. De Gennaro L, Marzano C, Cipolli C, Ferrara M (2012) How we remember the stuff that dreams are made of: neurobiological approaches to the brain mechanisms of dream recall. Behav Brain Res 226:592–596. doi: 10.1016/j.bbr.2011.10.017 CrossRefPubMedGoogle Scholar
  15. De Gennaro L, Lanteri O, Piras F, Scarpelli S, Assogna F, Ferrara M, Caltagirone C, Spalletta G (2016) Dopaminergic system and dream recall: an MRI study in Parkinson’s disease patients. Hum Brain Mapp 37:1136–1147. doi: 10.1002/hbm.23095 CrossRefPubMedGoogle Scholar
  16. Desseilles M, Dang-Vu TT, Sterpenich V, Schwartz S (2011) Cognitive and emotional processes during dreaming: a neuroimaging view. Conscious Cogn 20:998–1008. doi: 10.1016/j.concog.2010.10.005 CrossRefPubMedGoogle Scholar
  17. Domhoff GW (2003) The scientific study of dreams: Neural networks, cognitive development, and content analysis. APA Press, Washington. doi: 10.1037/10463-000 CrossRefGoogle Scholar
  18. Domhoff GW (2011) The neural substrate for dreaming: is it a subsystem of the default network?. Conscious Cogn 20:1163–1174. doi: 10.1016/j.concog.2011.03.001 CrossRefGoogle Scholar
  19. Doricchi F, Violani C (1992) Dream recall in brain-damage patients: a contribution to the neuropsychology of dreaming through a review of the literature. In: Antrobus JS, Bertini M (eds) The neuropsychology of sleep and dreaming. Erlbaum, Hillsdale, pp 99–129Google Scholar
  20. Eichenlaub JB, Bertrand O, Morlet D, Ruby P (2014a) Brain reactivity differentiates subjects with high and low dream recall frequencies during both sleep and wakefulness. Cereb Cortex 24:1206–1215. doi: 10.1093/cercor/bhs388 CrossRefPubMedGoogle Scholar
  21. Eichenlaub JB, Nicolas A, Daltrozzo J, Redouté J, Costes N, Ruby P (2014b) Resting brain activity varies with dream recall frequency between subjects. Neuropsychopharmacology 39:1594–1602. doi: 10.1093/cercor/bhs388 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Esposito MJ, Nielsen TA, Paquette T (2004) Reduced alpha power associated with the recall of mentation from stage 2 and stage REM sleep. Psychophysiology 41:288–297. doi: 10.1111/j.1469-8986.00143.x CrossRefPubMedGoogle Scholar
  23. Ferri R, Rundo F, Bruni O, Terzano MG, Stam CJ (2006) Regional scalp EEG slow-wave synchronization during sleep cyclic alternating pattern A1 subtypes. Neurosci Lett 404:352–357CrossRefPubMedGoogle Scholar
  24. Finelli LA, Borbély AA, Achermann P (2001) Functional topography of the human nonREM sleep electroencephalogram. Eur J Neurosci 13:2282–2290. doi: 10.1046/j.0953-816x.2001.01597.x CrossRefPubMedGoogle Scholar
  25. Foulkes D (1962) Dream reports from different stages of sleep. J Abnorm Soc Psychol 65:14–25CrossRefPubMedGoogle Scholar
  26. Foulkes D, Schmidt M (1983) Temporal sequence and unit composition in dream reports from different stages of sleep. Sleep 6:265–280CrossRefPubMedGoogle Scholar
  27. Giambra LM, Jung RE, Grodsky A (1996) Age changes in dream recall in adulthood. Dreaming 6:17–31. doi: 10.1037/h0094443 CrossRefGoogle Scholar
  28. Guderian S, Schott BH, Richardson-Klavehn A, Düzel E (2009) Medial temporal theta state before an event predicts episodic encoding success in humans. Proc Natl Acad Sci USA 106:5365–5370. doi: 10.1037/h0094443 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hobson JA, Hong CC, Friston KJ (2014) Virtual reality and consciousness inference in dreaming. Front Psychol 5:1133. doi: 10.3389/fpsyg.2014.01133 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Klimesch W (1996) Memory processes, brain oscillations and EEG synchronization. Int J Psychophysiol 24:61–100. doi: 10.1016/S0167-8760(96)00057-8 CrossRefPubMedGoogle Scholar
  31. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29:169–195. doi: 10.1016/S0165-0173(98)00056-3 CrossRefPubMedGoogle Scholar
  32. Klimesch W, Doppelmayr M, Russegger H, Pachinger T (1996) Theta band power in the human scalp EEG and the encoding of new information. Neuroreport 7:1235–1240CrossRefPubMedGoogle Scholar
  33. Koulack D, Goodenough DR (1976) Dream recall and dream recall failure: an arousal-retrieval model. Psychol Bull 83:975. doi: 10.1037/0033-2909.83.5.975 CrossRefGoogle Scholar
  34. Marzano C, Ferrara M, Mauro F, Moroni F, Gorgoni M, Tempesta D, Cipolli C, De Gennaro L (2011a) Recalling and forgetting dreams: theta and alpha oscillations during sleep predict subsequent dream recall. J Neurosci 31:6674–6683. doi: 10.1523/JNEUROSCI.0412-11.2011 CrossRefPubMedGoogle Scholar
  35. Marzano C, Ferrara M, Moroni F, De Gennaro L (2011b) Electroencephalographic sleep inertia of the awakening brain. Neuroscience 176:308–317. doi: 10.1016/j.neuroscience.2010.12.014 CrossRefPubMedGoogle Scholar
  36. Massimini M, Ferrarelli F, Sarasso S, Tononi G (2012) Cortical mechanisms of loss of consciousness: insight from TMS/EEG studies. Arch Ital Biol 150:44–55. doi: 10.4449/aib.v150i2.1361 PubMedGoogle Scholar
  37. Nielsen T (2012) Variations in dream recall frequency and dream theme diversity by age and sex. Front Neurol 3:106. doi: 10.3389/fneur.2012.00106 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ohayon MM, Carskadon MA, Guilleminault C, Vitiello MV (2004) Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. Sleep 27:1255–1274CrossRefPubMedGoogle Scholar
  39. Pace-Schott EF (2016) Exploring the brain bases of dreaming. Commentary on: “Beyond the neuropsychology of dreaming: insights into the neural basis of dreaming with new techniques of sleep recording and analysis”. Sleep Med Rev. doi: 10.1016/j.smrv.2016.11.005 PubMedGoogle Scholar
  40. Parrino L, Ferri R, Bruni O, Terzano MG (2012) Cyclic alternating pattern (CAP): the marker of sleep instability. Sleep Med Rev 16:27–45. doi: 10.1016/j.smrv.2011.02.003 CrossRefPubMedGoogle Scholar
  41. Perneger TV (1998) What’s wrong with Bonferroni adjustments. BMJ 316:1236–1238. doi: 10.1136/bmj.316.7139.1236 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pigorini A, Sarasso S, Proserpio P, Szymanski C, Arnulfo G, Casarotto S, Fecchio M, Rosanova M, Mariotti M, Lo Russo G, Palva JM, Nobili L, Massimini M (2015) Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. Neuroimage 112:105–113. doi: 10.1016/j.neuroimage.2015.02.056 CrossRefPubMedGoogle Scholar
  43. Pivik T, Foulkes D (1968) NREM mentation: relation to personality, orientation time, and time of night. J Consult Clin Psychol 32:144–151CrossRefPubMedGoogle Scholar
  44. Quercia A, Zappasodi F, Committeri G, Tamburro G, Pizzella V, Valentini M, Ferrara M (2014) Neurobehavioral performance during an intensive spatial navigation task and local use-dependent changes in the wake electroencephalogram. Conference Paper: 22th Congress of the European Sleep Research Society. doi: 10.1111/jsr.12213
  45. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. UCLA Brain Information Service, Los AngelesGoogle Scholar
  46. Rosenblatt SI, Antrobus JI, Zimler JP (1992) The effect of post-awakening differences in activation on the REM–NREM report effect and recall of information from films. In: Antrobus JS, Bertini M (eds) The neuropsychology of sleep and dreaming. Erlbaum, HillsdaleGoogle Scholar
  47. Ruby PM, Blochet C, Eichenlaub JB, Bertrand O, Morlet D, Bidet-Caulet A (2013) Alpha reactivity to first names differs in subjects with high and low dream recall frequency. Front Psychol 4:419. doi: 10.3389/fpsyg.2013.00419 PubMedPubMedCentralGoogle Scholar
  48. Sankoh AJ, Huque MF, Dubey SD (1997) Some comments on frequently used multiple endpoint adjustment methods in clinical trials. Stat Med 16:2529–2542. doi: 10.1002/(SICI)1097-0258(19971130)16:22<2529::AID-SIM692>3.0.CO;2- CrossRefPubMedGoogle Scholar
  49. Scarpelli S, Marzano C, D’Atri A, Gorgoni M, Ferrara M, De Gennaro L (2015a) State-or trait-like individual differences in dream recall: preliminary findings from a within-subjects study of multiple nap REM sleep awakenings. Front Psychol 6:928. doi: 10.3389/fpsyg.2015.00928 PubMedPubMedCentralGoogle Scholar
  50. Scarpelli S, D’Atri A, Gorgoni M, Ferrara M, De Gennaro L (2015b) EEG oscillations during sleep and dream recall: state- or trait-like individual differences?. Front Psychol 6:605. doi: 10.3389/fpsyg.2015.00605 PubMedPubMedCentralGoogle Scholar
  51. Schredl M (2009) Dreams in patients with sleep disorders. Sleep Med Rev 13:215–221. doi: 10.1016/j.smrv.2008.06.002 CrossRefPubMedGoogle Scholar
  52. Schredl M, Hofmann F (2003) Continuity between waking activities and dream activities. Conscious Cogn 12:298–308. doi: 10.1016/S1053-8100(02)00072-7 CrossRefPubMedGoogle Scholar
  53. Schredl M, Schäfer G, Weber B, Heuser I (1998) Dreaming and insomnia: dream recall and dream content of patients with insomnia. J Sleep Res 7:191–198. doi: 10.1046/j.1365-2869.1998.00113.x CrossRefPubMedGoogle Scholar
  54. Siclari F, LaRocque JJ, Bernardi G, Postle BR, Tononi G (2014) The neural correlates of consciousness in sleep: a no-task, within-state paradigm. bioRxiv. doi: 10.1101/012443 Google Scholar
  55. Simor P, Bódizs R, Horváth K, Ferri R (2013) Disturbed dreaming and the instability of sleep: altered nonrapid eye movement sleep microstructure in individuals with frequent nightmares as revealed by the cyclic alternating pattern. Sleep 36:413–419. doi: 10.5665/sleep.2462 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Strunz F (1993) Dreams in the elderly: contents and clinical usefulness. Gesundheitswesen 55(11):595–601 (in German)PubMedGoogle Scholar
  57. Takeuchi T, Ogilvie RD, Murphy TI, Ferrelli AV (2003) EEG activities during elicited sleep onset REM and NREM periods reflect different mechanisms of dream generation. Clin Neurophysiol 114:210–220. doi: 10.1016/S1388-2457(02)00385-1 CrossRefPubMedGoogle Scholar
  58. Taub JM (1971) Dreams recalled spontaneously following afternoon naps and nocturnal sleep. J Abnorm Psychol 178:229–231CrossRefGoogle Scholar
  59. Voss U, Holzmann R, Hobson A, Paulus W, Koppehele-Gossel J, Klimke A, Nitsche MA (2014) Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nat Neurosci 17:810–812. doi: 10.1038/nn.3719 CrossRefPubMedGoogle Scholar
  60. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G (2011) Local sleep in awake rats. Nature 472:443–447. doi: 10.1038/nature10009 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Whitten TA, Hughes AM, Dickson CT, Caplan JB (2011) A better oscillation detection method robustly extracts EEG rhythms across brain state changes: the human alpha rhythm as a test case. Neuroimage 54:860–874. doi: 10.1016/j.neuroimage.2010.08.064 CrossRefPubMedGoogle Scholar
  62. Zimmerman WB (1970) Sleep mentation and auditory awakening thresholds. Psychophysiology 6:540–549. doi: 10.1111/j.1469-8986.1970.tb02243.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Serena Scarpelli
    • 1
  • Aurora D’Atri
    • 1
  • Anastasia Mangiaruga
    • 1
  • Cristina Marzano
    • 1
  • Maurizio Gorgoni
    • 1
  • Cinzia Schiappa
    • 1
  • Michele Ferrara
    • 2
  • Luigi De Gennaro
    • 1
    Email author
  1. 1.Department of PsychologySapienza University of RomeRomeItaly
  2. 2.Department of Biotechnological and Applied Clinical SciencesUniversity of L’AquilaCoppitoItaly

Personalised recommendations