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Research Article

Evidence for the Re-Enactment of a Recently Learned Behavior during Sleepwalking

  • Delphine Oudiette equal contributor mail,

    equal contributor Contributed equally to this work with: Delphine Oudiette, Irina Constantinescu

    isabelle.arnulf@psl.aphp.fr

    Affiliations: Sleep Disorders Unit, Pitié-Salpêtrière Hospital, APHP, Paris, France, Université Pierre et Marie Curie-Paris6, Centre de Recherche de l'Institut du Cerveau et de la Moelle epiniere, UMR-S975, Paris, France

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  • Irina Constantinescu equal contributor,

    equal contributor Contributed equally to this work with: Delphine Oudiette, Irina Constantinescu

    Affiliations: Department of Neuroscience, and Geneva Neuroscience Center, University of Geneva, Geneva, Switzerland, Swiss Center for Affective Sciences (NCCR), University of Geneva, Geneva, Switzerland

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  • Laurène Leclair-Visonneau,

    Affiliations: Sleep Disorders Unit, Pitié-Salpêtrière Hospital, APHP, Paris, France, Université Pierre et Marie Curie-Paris6, Centre de Recherche de l'Institut du Cerveau et de la Moelle epiniere, UMR-S975, Paris, France

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  • Marie Vidailhet,

    Affiliations: Inserm, U975, Paris, France, Université Pierre et Marie Curie-Paris6, Centre de Recherche de l'Institut du Cerveau et de la Moelle epiniere, UMR-S975, Paris, France

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  • Sophie Schwartz,

    Affiliations: Department of Neuroscience, and Geneva Neuroscience Center, University of Geneva, Geneva, Switzerland, Swiss Center for Affective Sciences (NCCR), University of Geneva, Geneva, Switzerland

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  • Isabelle Arnulf

    Affiliations: Sleep Disorders Unit, Pitié-Salpêtrière Hospital, APHP, Paris, France, Inserm, U975, Paris, France, Université Pierre et Marie Curie-Paris6, Centre de Recherche de l'Institut du Cerveau et de la Moelle epiniere, UMR-S975, Paris, France

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  • Published: March 21, 2011
  • DOI: 10.1371/journal.pone.0018056

Reader Comments (1)

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Data Does Not Support Conclusions of Re-inactment of Waking Memories During Sleepwalking Or RBD (with authors names attached)

Posted by pressm on 10 May 2011 at 14:24 GMT

The article by Oudiette et al represents a rare attempt to directly test a memory theory in humans while they sleep. While we certainly encourage such direct experiments, we must respectfully disagree with the authors’ assumptions, methods and most importantly - conclusions.

1. Initial assumptions are not supported by the scientific literature. Dreamers do not frequently incorporate events from the previous day. A recent review of dreaming and the brain stated:

“ Whereas ‘residues’ from waking experience are incorporated in ~ 50% of dreams, they do so in new and unrelated contexts, and verified memories for episodes of recent life are only found in ~ 1.5% of dreams” (Nir & Tononi, 2011)

Furthermore, no more than 20% of dream material is in any way related to what the dreamer recollects of events in his or her life history.(Fosse, M.J., Fosse, R., Hobson, J.A., Stickgold, R. J., “Dreaming and Episodic Memory: A Functional Dissociation?”, J. Cogn. Neurosci. 15, 1-9, 2003)

2. The rationale for testing sleepwalkers and RBD patients in this protocol is clear. They are only sleepers who exhibit behavior during or out of sleep. However, these behaviors, in this group of patients, may not be representative of normal neural processes during sleep. RBD is often associated with progressive degenerative processes in the brain. Sleepwalking is also associated with functional abnormalities of brain function during sleep. Thus, these groups may not be representative of typical brain function during sleep.

3. Complex behaviors occurring out of NREM sleep rarely occur on a nightly basis. In neuronal processes of activation and demodulation necessary for state declaration, a host of factors conspire to create the “perfect storm” required for the expression of sleepwalking or confusional arousals. Sleepwalking in adults typically occurs infrequently. Further, sleepwalking episodes rarely occur in the sleep laboratory even in individuals who report frequent episodes at home. Any future studies would appear to require employment of techniques to directly trigger complex behaviors or at least consider developing new tools to longitudinally monitor for such behaviors. Automated video tracking systems have become relatively common place in assessing behavior in animal research. Systems, such as Ethovision, offer algorithms for objective pattern analysis and allow the study of behaviors that occur briefly which are interspersed with long periods of inaction. Automated video tracking systems have been used to compare changes in behavioral characteristics under a variety of conditions as diverse as aquariums with zebrafish and in various animal models, including knockout mice (Ref. Example: “Taylor G. et all, Behavioral Characterization of P311 Knockout Mice”, , Genes, Brain, & Behavior, 2008, 7: 786-795) Whether such tools can be applied in human research in both a practical and cost effective manner has yet to be determined.

4. The methods sections states 11 individuals were used as judges. What were the qualifications of these individuals? Why 11? Was there a standard method used in evaluating the videos? Were the judges taught this method? Did the judges have to show a certain level of performance, inter-judge agreement? The described method does not appear to have been constructed in response to statistical requirements in order to insure reliability or validity.

5. The author’s conclusions are not supported by their results. In the final sentence of their article they state

“Our work therefore demonstrates that parasomnias such as sleepwalking and REM sleep behavior disorder are useful neurological models for studying cognitive functions during sleep, and may for example motivate further investigations on the respective contribution of non REM and REM sleep on learning and brain plasticity (p. 7)

In fact, their techniques were completely unsuccessful in patients in RBD and produced only a single possibly positive episode in the sleepwalkers.

(Sleepwalkers N=19, 12 had single night PSGs, 7 had double night PSGs, Total PSGs = 12+14=26).
(RBD N=20, 13 had single night PSGs, 7 had double night PSGs, Total PSGs = 13 + 14=27).
Total PSG for the Sleepwalkers + RBD = 26 + 27 = 53

#Positive Response=1
1/53=1.89%

Sleepwalkers and RBD patients may yet be proven to be good subjects for this type of experimentation, but this report suggests the exact opposite is likely to be true.

6. Whether dreams have no function and are a spandrels of the mind that are but by-products of the evolution of sleep and consciousness (Foulkes, D., Dreaming: A Cognitive-Psychological Analysis, Lawrence Erlbaum Associates (1985), Domhoff, G.W., The Scientific Study of Dreams: Neural Networks, Cognitive Development, And Content Analysis, American Psychological Association (2003) ) or that dreams may serve a creative function through protoconsciousness where the brain is preparing itself for integrative functions including learning (Hobson- Ref: Hobson, J.A., “REM Sleep and Dreaming: Towards a Theory of Protoconsciousness”, Nature Reviews, 1 October 2009) remains open for active debate and investigation. However, given recent technical advances in neuroscience that can discern the functional networks underlying dreaming, interpretation via free association, once popularized by Freud, should be discouraged in the neuroscience of dream research. In the subsection on “Dreams content after the post-training night of sleep”, the authors note that a subject had a “cross” dream involving two diagonal paths. Though this subject did not engage in any replay of learned behaviors during sleepwalking, it is implied that this “cross” dream was reflective of the previously reinforced learned behavior now being experienced during sleep. Such references appear to introduce an unfounded bias as the “cross” metaphor is ubiquitous and as such is malleable in its meaning depending upon the condition. Interpretation via free association would appear to introduce a situation that is neither provable if true nor falsifiable if false.

7. The authors conclusions that daytime waking activities may find their way into complex behaviors of sleepwalkers the following night via “re-enactment” is likely to be misconstrued in forensic settings in which a sleepwalking defense is presented for criminal activities. In a famous sleepwalking case in Arizona in 1999 (Arizona v. Scott Falater), there was testimony that a defendant who stabbed his wife 44 times, ostensively while sleepwalking, was actually reenacting or completing an interrupted behavior during wakefulness earlier in the day. This testimony was intended to support the contention that the defendant had been sleepwalking when he killed his wife. This theory of the crime was presented even though in a published article about in an earlier Canadian sleepwalking defense case, some of the same expert witnesses had written that

“There is no evidence that a somnambulist during sleepwalking can either execute a conscious intent from prior wakefulness or can create an intent”. (Broughton 1994)

It should be clear from our comments above that in our opinion this article does not constitute scientific support for theories linking sleepwalking episodes REM sleep related dreaming to earlier waking behaviors and that earlier waking behaviors are irrelevant in forensic sleepwalking cases. This is simply a negative study.


Mark R. Pressman, Ph.D.

Diplomate, American Board of Sleep Medicine,
Sleep Medicine Services, Lankenau Medical Center and Lankenau Institute for Medical Research
Lancaster Avenue, Wynnewood, PA 19096, USA
Jefferson Medical College, Philadelphia, PA USA
E-mail address: pressmanm@mlhs.org

Michel Cramer Bornemann, M.D.
Mark W. Mahowald, M.D.

Diplomates, American Board of Sleep Medicine,
Minnesota Regional Sleep Disorders Center,
Department of Neurology, Hennepin County Medical
Center,
Minneapolis, MN, USA
University of Minnesota Medical School,
Minneapolis, MN, USA

No competing interests declared.