Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep.

Recent studies indicated a selective activation during rapid eye movement (REM) sleep of the amygdala known to play a decisive role in the processing of emotional stimuli. This study compared memory retention of emotional versus neutral text material over intervals covering either early sleep known to be dominated by nonREM slow wave sleep (SWS) or late sleep, in which REM sleep is dominant. Two groups of men were tested across 3-h periods of early and late sleep (sleep group) or corresponding retention intervals filled with wakefulness (wake group). Sleep was recorded polysomnographically. Cortisol concentrations in saliva were monitored at acquisition and retrieval testing. As expected, the amount of REM sleep was about three times greater during late than during early retention sleep, whereas a reversed pattern was observed for SWS distribution (P < 0.001). Sleep improved retention, compared with the effects of wake intervals (P < 0.02). However, this effect was substantial only in the late night (P < 0.005), during which retention was generally worse than during the early night (P < 0.02). Late sleep particularly enhanced memory for emotional texts. This effect was highly significant in comparison with memory for neutral texts (P < 0.01) and in comparison with memory after late and early wake intervals (P < 0.001). Cortisol concentration differed between early and late retention intervals but not between sleep and wake conditions. Results are consonant with a supportive function of REM sleep predominating late sleep for the formation of emotional memory in humans.

[1]  K. M. Dallenbach,et al.  Obliviscence During Sleep and Waking. , 1924 .

[2]  Foulkes Wd Dream reports from different stages of sleep. , 1962 .

[3]  B. Ekstrand Effect of sleep on memory. , 1967, Journal of experimental psychology.

[4]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[5]  J. A. C. EMPSON,et al.  Rapid Eye Movements and Remembering , 1970, Nature.

[6]  B. Ekstrand,et al.  Effect of sleep on memory. II. Differential effect of the first and second half of the night. , 1971, Journal of experimental psychology.

[7]  R. Greenberg,et al.  The adaptive function of sleep: the differential effects of sleep and dreaming on recall. , 1972, Journal of abnormal psychology.

[8]  T. R. Barrett,et al.  Effect of sleep on memory: III. Controlling for time-of-day effects , 1972 .

[9]  B. Ekstrand,et al.  Sleep and Memory , 1973, Science.

[10]  H. A. Witkin,et al.  The effects of stress films on dream affect and on respiration and eye-movement activity during Rapid-Eye-Movement sleep. , 1975, Psychophysiology.

[11]  I. Lewin,et al.  The effect of REM deprivation: is it detrimental, beneficial, or neutral? , 1975, Psychophysiology.

[12]  R. Cartwright,et al.  Effects of REM time on what is recalled. , 1975, Psychophysiology.

[13]  T. R. Barrett,et al.  THE EFFECT OF SLEEP ON HUMAN LONG-TERM MEMORY , 1977 .

[14]  M. Stones Memory performance after arousal from different sleep stages. , 1977, British journal of psychology.

[15]  A. Tilley,et al.  REM sleep and memory consolidation , 1978, Biological Psychology.

[16]  L. Scrima Isolated REM sleep facilitates recall of complex associative information. , 1982, Psychophysiology.

[17]  A. Tilley,et al.  Retrieval from semantic memory at different times of day. , 1983, Journal of experimental psychology. Learning, memory, and cognition.

[18]  J. A. Horne,et al.  The consolidation hypothesis for REM sleep function: Stress and other confounding factors — A review , 1984, Biological Psychology.

[19]  Carlyle Smith,et al.  Sleep states and learning: A review of the animal literature , 1985, Neuroscience & Biobehavioral Reviews.

[20]  Daniel Reisberg,et al.  Remembering emotional events , 1992, Memory & cognition.

[21]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[22]  L. Squire Declarative and Nondeclarative Memory: Multiple Brain Systems Supporting Learning and Memory , 1992, Journal of Cognitive Neuroscience.

[23]  R. Thisted,et al.  Sleep and Psychiatric Disorders: A Meta-analysis , 1992 .

[24]  James L. McGaugh,et al.  β-Adrenergic activation and memory for emotional events , 1994, Nature.

[25]  J. Kessler,et al.  The amygdala's contribution to memory—a study on two patients with Urbach-Wiethe disease , 1994 .

[26]  James L. McGaugh,et al.  The amygdala and emotional memory , 1995, Nature.

[27]  Carlyle T. Smith,et al.  Sleep states and memory processes , 1995, Behavioural Brain Research.

[28]  J. Calvo,et al.  Prolonged enhancement of REM sleep produced by carbachol microinjection into the amygdala , 1996, Neuroreport.

[29]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  W Wippich,et al.  Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. , 1996, Life sciences.

[31]  C. Degueldre,et al.  Functional neuroanatomy of human rapid-eye-movement sleep and dreaming , 1996, Nature.

[32]  J. D. McGaugh,et al.  Involvement of the amygdala in memory storage: interaction with other brain systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Rina Schul,et al.  Impaired declarative memory for emotional material following bilateral amygdala damage in humans. , 1997 .

[34]  D. Koulack Recognition Memory, Orcadian Rhythms, and Sleep , 1997, Perceptual and motor skills.

[35]  J. D. McGaugh,et al.  Intact enhancement of declarative memory for emotional material in amnesia. , 1997, Learning & memory.

[36]  J. D. McGaugh,et al.  Glucocorticoid Receptor Agonist and Antagonist Administration into the Basolateral but Not Central Amygdala Modulates Memory Storage , 1997, Neurobiology of Learning and Memory.

[37]  J. Born,et al.  Effects of Early and Late Nocturnal Sleep on Declarative and Procedural Memory , 1997, Journal of Cognitive Neuroscience.

[38]  D. Kupfer,et al.  Forebrain activation in REM sleep: an FDG PET study 1 Presented in abstract form at the Society for Neuroscience Meeting, 1996. 1 , 1997, Brain Research.

[39]  Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats. , 1998, Behavioral neuroscience.

[40]  James L. McGaugh,et al.  Stress and glucocorticoids impair retrieval of long-term spatial memory , 1998, Nature.

[41]  M. Thase,et al.  Depression, sleep, and antidepressants. , 1998, The Journal of clinical psychiatry.

[42]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[43]  Expression in paradoxical sleep of a conditioned heart rate response. , 1999, Neuroreport.

[44]  J. Born,et al.  Effects of early and late nocturnal sleep on priming and spatial memory. , 1999, Psychophysiology.

[45]  J. D. McGaugh,et al.  Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: involvement of the basolateral amygdala , 1999, The European journal of neuroscience.

[46]  J. Born,et al.  Dexamethasone blocks sleep induced improvement of declarative memory , 1999, Psychoneuroendocrinology.

[47]  J. Newcomer,et al.  Decreased memory performance in healthy humans induced by stress-level cortisol treatment. , 1999, Archives of general psychiatry.

[48]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[49]  R. Vertes,et al.  The case against memory consolidation in REM sleep , 2000, Behavioral and Brain Sciences.

[50]  R. Adolphs,et al.  Impaired emotional declarative memory following unilateral amygdala damage. , 2000, Learning & memory.

[51]  Benno Roozendaal,et al.  Glucocorticoids and the regulation of memory consolidation , 2000, Psychoneuroendocrinology.

[52]  J. Hobson,et al.  Visual Discrimination Task Improvement: A Multi-Step Process Occurring During Sleep , 2000, Journal of Cognitive Neuroscience.