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Robert Stickgold Sleep, Memory and Dreams: Putting It All Together

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Sleep, Memory and Dreams: Putting It All Together OHSU Brain Institute, Portland OR April 2017 Robert Stickgold Harvard Medical School Beth Israel Deaconess Medical Center Boston, MA Some of the work presented here was sponsored by Sepracor, Inc. Today’s Outline 1) The physiology of sleep 2) The diversity of memory evolution a) Stabilization and enhancement b) Selection, gist, rules and insight 3) Sleep, memory and dreams 4) Sleep and psychiatric disorders The Physiology and Chemistry of the Brain Change Across the Night A Good Night’s Sleep REM sleep Wake I/REM II III Stage 2 NREM IV SWS 11 PM 1 AM 3 AM 5 AM 7 AM Sleep Physiology EEG Wake Stage 2 Stage 4 REM 2 sec EOG Stage 1 Stage 2 REM EMG Wake Stage 4 REM Neuromodulation Varies Across the Wake-Sleep Cycle Active Quiet SWS REM Wake Wake ACh NE 5-HT Ach: Atropine (belladonna) and scopolamine NE: MAO inhibitors, cocaine 5-HT: SSRI’s, LSD Regional Activation in REM Sleep Sleep Balances Emotional Memories Emotional Words • Peter Hu • Matt Walker Emotional Memory After Sleep Deprivation Neutral, Negative, Positive Sleep No Sleep Negative Stimuli amygdala mOFC Yoo et al. (2007) Curr Biol 17, R877-878 Emotional Memory After Sleep Deprivation encoding test Sleep Sleep Sleep No Sleep Sleep Sleep Emotional Memory After Sleep Deprivation Sleep Deprived Memory Recognition Memory positive neutral negative Sleep and Memory Evolution Stabilization & Enhancement Sleep Enhances Procedural Learning 1 2 3 4 • Matthew Walker • Tiffany Brakefield Sequence • Alexandra Morgan 4-1-3-2-4 Sleep Enhances Procedural Learning 1 2 3 4 • Matthew Walker • Tiffany Brakefield Sequence • Alexandra Morgan 4-1-3-2-4 Learning Rate Saturates Rapidly 24 20 16 # Sequences / sec 30 # Sequences 10 PM 12 10 AM 1 2 3 4 5 6 7 8 9 10 11 12 Training Trials Baseline (lasting 12 mins) Post-training Walker et al. Neuron 35, 205 (2002) Motor Sequence Learning 28 28 p<0.0001 26 26 n.s. 24 24 # Sequences # Sequences / 30 sec 22 22 20 20 10AM 10PM 10PM 10AM SLEEP Walker et al. Neuron 35, 205 (2002) Sleep and Memory Evolution Salience, Gist, Rules, Insight (four examples) Sleep Consolidates Emotional Memory Emotional Trade-Off • Jessica Payne • Elizabeth Kensinger Emotional Trade-off 100 Neutral Emotional 90 Objects 80 Backgrounds 70 Items Recognized Items(%) Recognized 60 50 30 min 30 min Changes Over 12 Hr Wake or Sleep Neutral Scenes Emotional Scenes n.s. n.s. 0 Objects Backgrounds -4 -8 Change from Change from 30 min (%) -12 12 hr 12 hr 12 hr 12 hr wake sleep wake sleep Sleep Consolidates Episodic Declarative Memory Verbal Memory Task Word Lists Door House Ledge Glass Open Breeze • Jessica Payne Pane Frame Curtain • Ruth Propper Shade View nurse sick lawyer medicine health hospital stethoscopephysicianmedicinehospitallawyerpatientdentistdoctorcottonhealthofficenursetablesickill+ dentist physician ill patient office stethoscope D-R-M: 12-Hour Deterioration 15 Sleep Wake 0 -15 -30 * -45 % Change (relative % min Change 20to (relative * -60 Studied Gist words words Payne et al., Neurobiol Learn Mem 92, 327 (2009) Sleep Enhances Rules Weather Prediction Task • Ina Djonlagic • Andy Rosenfeld • Murray Barsky Probabilistic Learning Card 1 Card 2 Card 3 Card 4 80% 60% 40% 20% ?!? Djonlagic et al., Learn Mem 16, 751 (2009) Sleep Enhances Performance p = 0.01 Wake 14 Sleep 12 10 8 6 Improvement Improvement (% of trials) 4 2 0 Observation Djonlagic et al., Learn Mem 16, 751 (2009) Sleep Enhances Insight Number Reduction Task 1 1 4 4 9 4 9 4 • Ulrich Wagner 1 9 1 4 4 1 9 • Jan Born Wagner et al. (2004) Nature 427: 352 Development of Insight 1 1 4 4 9 4 9 4 1 9 1 4 4 1 9 60% 40% 20% Subjects gaining insight gaining Subjects 0% Wake/ Wake/ Sleep/ Day Night Night Sleep, Memory and Dreams New Experiences are Replayed at Sleep Onset Hypnagogic dreams • April Malia • Denise Maguire • David Roddenberry • Karen Emerge • Laura Babkes Hypnagogic Images of Tetris Group (n) Nights % Ss % Rpts Novices 2 75% 10.4% Experts 2 or 3 50% 4.7% Reports of Tetris Imagery NOVICE “Just seeing Tetris shapes floating around in my head like they could in the game, falling down, sort of putting them together in my mind” (JEG - Day 2) EXPERT “…seeing in my mind how the game pieces kind of float down and fit into the other pieces and am also rotating them” (TRP - Day 2) Hypnagogic Images of Tetris Group (n) Nights % Ss % Rpts Novices 2 75% 10.4% Experts 2 or 3 50% 4.7% Amnesiacs 3 60% 7.4% Reports of Tetris Imagery NOVICE “Just seeing Tetris shapes floating around in my head like they could in the game, falling down, sort of putting them together in my mind” (JEG - Day 2) EXPERT “…seeing in my mind how the game pieces kind of float down and fit into the other pieces and am also rotating them” (TRP - Day 2) AMNESIAC “I see images that are turned on their side. I don’t know what they are from, I wish I could remember, but they’re like blocks” (JEG - Day 2) Dream Content Predicts Sleep-Dependent Consolidation NREM Napping NYTime.com April 22, 2010 • Erin Wamsley • Matt Tucker Train ± NREM Test Nap 12 pm 2 4 6 pm p=.01 150 100 50 0 Improvement Improvement (sec) -50 -100 WAKE SLEEP (n=16) (n=16) Wamsley et al. Curr Biol 20, 850 (2010) Train ± NREM Test Nap 12 pm 2 4 6 pm REPORTS p=.01 400 p=0.0003 150 Not maze related 100 300 Maze related 50 200 0 n.s. 100 Improvement (sec) Improvement Improvement (sec) -50 0 -100 WAKE SLEEP WAKE SLEEP (n=16) (n=16) Wamsley et al. Curr Biol 20, 850 (2010) Quiet wakefulness (useful?) “I was thinking about the game that I used to play in high school, “Counter-Strike”, because of the same layout . and also I was just planning, and trying to remember the maze and trying to figure out the route” “ . thinking [about] what we have to do in the second maze test . wondered if it was going to be, like, the same . .” 400 p=0.0003 Dream reports (useless?) Not maze related 300 Maze related “I was thinking about the maze and kinda having people as check points, I guess, and 200 then that led me to think about when I went on this trip few years ago and we went to n.s. see these bat caves, and they're kind of like, 100 maze-like” Improvement Improvement (sec) “Looking for something” in a maze 0 “Just hearing the music” from the task WAKE SLEEP Wamsley et al. Curr Biol 20, 850 (2010) Sleep-Dependent Memory Processing: A Whole-Brain Process Hippocampus • Stabilization and enhancement • Salience selection Neocortex • Rule and gist extraction • Network integration Imagined scenarios DREAMING Narrative development Future projection Sleep & Psychiatry Schizophrenia and PTSD Sleep-Dependent Learning is Impaired in Schizophrenia (Study funded by Sepracor & Co.) • Dara Manoach • Erin Wamsley • Ann Shinn • Donald Goff Motor Skill Learning in Chronic Schizophrenia 21 16 14 19 # Sequences / 30 sec 17 12 sec (controls) 15 10 13 8 (SZ) # Sequences / 30 11 6 9 4 2 4 6 8 10 12 2 4 6 8 10 12 Trials Manoach et al. Biol Psychiatry 56, 951 (2004) Stage 2 NREM Spindles in SZ and Controls p < .0001) ) 2.0 1 - 1.5 1.0 Spindle density (min density Spindle 0.5 Controls SZ Manoach et al. Biol Psychiatry 56, 951 (2004) Spindle Sigma Power Wamsley et al. Sleep 36, 1369 (2013) Impact of Eszopiclone 30 * 25 20 * 15 10 5 Overnight Improvement (%) Improvement Overnight 0 baseline baseline placebo eszopiclone Controls Schizophrenia patients Wamsley et al. Sleep 36, 1369 (2013) Spindle Sigma Power Wamsley et al. Sleep 36, 1369 (2013) Improvement and Stage 2 NREM 60% 40% 20% % Initial % Initial improvement 0% Young controls SZ pts w/ eszopiclone -20% 20 40 60 80 100 % Stage 2 NREM sleep – 4th Quarter PTSD A Disorder of Sleep-Dependent Memory Evolution PTSD – What is it? Sleep! Traumatic Trauma Processing Trauma Event Memory Resolution ? (the therapist’s job!) Stasis PTSD Stickgold (2002) J Clin Psychol 58, 61–75 Trauma Resolution and Sleep-Dependent Memory Evolution The normal resolution of trauma requires: • Normalizing emotional memories • Separating emotions from their contexts • Extracting gist representations and rules • Integrating the trauma memory with older memories • Gaining insight This memory processing occurs preferentially in REM sleep, which guide the evolution of memories over time Stickgold (2002) J Clin Psychol 58, 61–75 PTSD – A Failure of Sleep-Dependent Memory Evolution When processes involved in the normal sleep- dependent evolution of trauma memories fail, PTSD may inevitably follow. Stickgold (2002) J Clin Psychol 58, 61–75 Summary • Sleep plays a critical role in the evolution of memories, stabilizing and strengthening them. • But it also identifies, analyzes, and maintains our most important memories, finding patterns in them, extracting gist and facilitating insight. • Disruption of these processes may contribute to psychiatric disorders, including SZ and PTSD. But perhaps more importantly, these systems carry out what may well be the most sophisticated function that the human brain performs – the building of models of ourselves and our world, providing clues to the course of our future and creating the very meaning of our lives. .
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