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How Developmental Changes in Sleep Biology May Affect ... · How Developmental Changes in Sleep...
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How Developmental Changes in Sleep Biology May Affect Adolescent Behavior
Mary A. Carskadon, PhD Sleep for Science Research Lab
EP Bradley Hospital Alpert Medical School of Brown University
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Conflict of Interest
• none
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Sleep propensity increases as
waking accumulates and dissipates with sleep
Sleep propensity oscillates with a daily (circadian) variation
From: Borbely AA. Human Frontier Science Program, 2000.
Sle
ep P
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Sle
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Observed features of the clock during adolescence
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Species Manifesting Juvenile Phase Delay
• Homo sapiens (humans) • Macca mulatta (Rhesus monkeys) • Octodon degus (degu) [some ?] • Rattus norvegicus (laboratory rat) • Mus musculus (laboratory mouse) • Psammomys obesus (fat sand rat)
Hagenauer et al., Devel Neurosci, 2009
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Phase Preference in 6th Graders
F(2,263) = 3.12 p<.05 F(1,175) = 3.46 p<.10
Carskadon, Vieira & Acebo Sleep 1993
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Chronotype and Adolescence
Roenneberg et al., Current Biol., 2004
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Melatonin Onset (DLMO) Phase and Puberty Stage
Carskadon et al. NYAS, 2004
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Activity offset delays in pubertal Macaques
• Puberty: phase delay in
the daily offset of activity
• If puberty is inhibited by zinc deprivation, the phase delay does not occur.
Average time of 1st Menarche
Average time of 1st ovulation = 44m
Golub et al., In: Adolescent development…, 2002
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Pubertal Phase Delay in Degus
• Activity onset delays at puberty in both males and females
First preputial and vaginal openings develop at about 8-14 weeks
Hummer et al., 2007
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What might underlie/support/influence a phase delay?
• Changes in light exposure
– Staying up later // more late light – Waking up later // less morning light
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Adolescent Self-Report
Bedtime
Risetime
Jenni & Carskadon, SRS BSG, 2005
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What might underlie phase delay?
• Changes in light exposure – Staying up later // more late light – Waking up later // less morning light
• Change in phase-dependent sensitivity to light exposure
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Exaggerated phase delay to light in pubertal female mice
Hagenauer et al., Devel Neurosci, 2001; after Weinert & Kompaeurova, Zoology, 1998
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What might underlie phase delay?
• Changes in light exposure – Staying up later // more late light – Waking up later // less morning light
• Change in phase-dependent sensitivity to light exposure
• Longer intrinsic circadian period (i.e., longer internal day length)
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Longer Period = Later Phase
Hagenauer et al., Devel Neurosci, 2009
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Intrinsic Period
Adolescents
Adults
#
Intrinsic Circadian Period: Adolescents vs. Adults
Carskadon & Acebo Sleep, 2005
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What might underlie phase delay?
• Changes in light exposure – Staying up later // more late light – Waking up later // less morning light
• Change in phase-dependent sensitivity to light exposure
• Longer intrinsic circadian period (i.e., longer internal day length)
• Diminished amplitude of the circadian rhythm
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Salivary Melatonin Amplitude
Crowley et al., Dev Psychobiol, 2011
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Circadian Rhythms Summary
• Phase is delayed during adolescent development – Phase preference (chronotype) is later – Melatonin phase is later
• Phase-dependent light sensitivity may change • Intrinsic period in adolescents may affect phase • Reduced amplitude of the circadian clock may
dampen the signal for sleep
• Result: late nights are favored (so, too, late mornings)
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Features of Adolescent Sleep-Wake Homeostasis (Human)
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Sleep deprivation
Model
Night 1
Night 1
Night 2
Night 2
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Adolescent Brain Changes
Density of neuronal connections, cerebral metabolic rate, and brain wave amplitude decline during adolescence
Feinberg et al., J Theor Biol.,1990
Cerebral metabolic rate
Cortical synaptic density
Delta wave amplitude
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Tarokh & Carskadon, Encyclopedia of Neuroscience, 2009
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Jenni & Carskadon Sleep, 2004
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Sleep phenomenology changes; does sleep regulation?
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Sleep pressure dissipation does not change in adolescence
• SWA dissipation is unchanged across pubertal development
Jenni & Carskadon, Sleep 2004
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Across pubertal development, SWA accumulation rate changes
Jenni, Achermann & Carskadon Sleep, 2005
7.7 h
13.5 h
3.0 h
2.9 h
td = 2.8 h td = 2.7 h Decay Time Constant ti = 8.9 h ti = 12.1 h Rise Time Constant
Tanner Stages 1/2 Tanner Stage 5
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Sleep tendency & extended wakefulness
Taylor et al., J Sleep Res, 2005
Hours Awake 2.5 6.5 10.5 14.5 18.5 22.5 26.5
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Model of Process S in Development
Jenni & LeBourgeois Curr Op Psychiatry, 2006
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Summary of Process S Change
• Recovery sleep process does not change across adolescence – Need for sleep is stable
• Accumulation of sleep pressure slows – Staying awake longer is easier
• Result: late nights are easier to achieve, but the same amount of sleep is needed
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Adolescent Sleep Behavior
• Bedtime becomes later • Rise time becomes earlier (school dependent) • Total amount of sleep is reduced • Chronic insufficient sleep has its strongest
effects on sleepiness in the morning, especially if waking at an adverse circadian phase
• Evening alertness is bolstered by the clock-dependent alerting signal
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MSLT in high school students
• 10th grade • Start time = 0720 • No schedule
manipulation • Sleeping about 7
hours a night
Carskadon et al. Sleep, 1998
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Sle
ep
REM occurred in 12 of 25 subjects—most in the morning
REM sleep tendency also affected
Carskadon et al. Sleep, 1998
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Consequences of Clock/Homeostasis/Lifestyle Interaction
• Variable sleep timing
– Social Jet Lag (á la Roenneberg, Curr Biol, 2012)
• Chronic insufficient sleep • Deficits in mood, learning, impulse control,
etc. • Excessive sleepiness
& possible caffeine use?
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Caffeinated Beverage Daily
Falle
n as
leep
in sc
hool
NSF Sleep in America Poll, 2006
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Carskadon, Pediatr Clin North Am, 2011 © M.A. Carskadon
Greater sleepiness and more caffeine
use?
Evening caffeinated beverages disturb
sleep?
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A sampling of gaps…
• What affect do caffeinated energy drinks have on nighttime sleep?
• Do caffeinated energy drinks affect circadian rhythms?
• What is the impact of caffeinated energy drinks on alertness, performance, attention, and learning acquisition in the daytime?
• Do these beverages affect sleep-dependent learning?
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Acknowledgements Collaborators/Fellows Ron Seifer, PhD Christine Acebo, PhD Oskar G. Jenni, MD Peter Achermann, PhD Leila Tarokh, PhD Eliza Van Reen, PhD Katherine Sharkey, MD, PhD John McGeary, PhD Valerie Knopik, PhD Brandy Roane, PhD David Barker, PhD
Research Assistants Dave Bushnell Maggie Gordon-Fogelson Jena Burgner Gretchen Surhoff Erin Campopiano James Bass Sharon Driscoll
Lab Staff Katie Esterline Ellyn Ferriter Jon Lassonde Denise Maceroni Caroline Gredvig-Ardito
Summer Research Apprentices!
Funding Sources MH52415 MH01358 MH58879 AA13252 MH076969 Periodic Breathing Foundation