Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-04T21:50:31.627Z Has data issue: false hasContentIssue false

Effects of slow-wave activity on mood disturbance in major depressive disorder

Published online by Cambridge University Press:  29 May 2018

Jennifer R. Goldschmied*
Affiliation:
Center for Sleep & Circadian Neurobiology, University of Pennsylvania, 125 S.31st St, Philadelphia, PA 19104, USA
Philip Cheng
Affiliation:
Sleep Disorders and Research Center, Henry Ford Health System, 39450 W 12 Mile Rd, Novi MI 48377, USA
Robert Hoffmann
Affiliation:
Department of Psychiatry, University of Michigan, 4250 Plymouth Rd, Ann Arbor, MI 48109, USA
Elaine M. Boland
Affiliation:
Behavioral Health Service, Cpl. Michael J. Crescenz VA Medical Center, 3900 Woodland Ave., Philadelphia, PA 19104, USA
Patricia J. Deldin
Affiliation:
Department of Psychiatry, University of Michigan, 4250 Plymouth Rd, Ann Arbor, MI 48109, USA
Roseanne Armitage
Affiliation:
Department of Psychiatry, University of Michigan, 4250 Plymouth Rd, Ann Arbor, MI 48109, USA
*
Author for correspondence: Jennifer R. Goldschmied, E-mail: jrgolds2@pennmedicine.upenn.edu

Abstract

Background

Studies have demonstrated that decreases in slow-wave activity (SWA) predict decreases in depressive symptoms in those with major depressive disorder (MDD), suggesting that there may be a link between SWA and mood. The aim of the present study was to determine if the consequent change in SWA regulation following a mild homeostatic sleep challenge would predict mood disturbance.

Methods

Thirty-seven depressed and fifty-nine healthy adults spent three consecutive nights in the sleep laboratory. On the third night, bedtime was delayed by 3 h, as this procedure has been shown to provoke SWA. The Profile of Mood States questionnaire was administered on the morning following the baseline and sleep delay nights to measure mood disturbance.

Results

Results revealed that following sleep delay, a lower delta sleep ratio, indicative of inadequate dissipation of SWA from the first to the second non-rapid eye movement period, predicted increased mood disturbance in only those with MDD.

Conclusions

These data demonstrate that in the first half of the night, individuals with MDD who have less SWA dissipation as a consequence of impaired SWA regulation have greater mood disturbance, and may suggest that appropriate homeostatic regulation of sleep is an important factor in the disorder.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Retired.

References

Antonijevic, IA, Stalla, GK and Steiger, A (2000) Modulation of the sleep electroencephalogram by estrogen replacement in postmenopausal women. American Journal of Obstetrics and Gynecology 182, 277282.Google Scholar
Armitage, R (2007) Sleep and circadian rhythms in mood disorders. Acta Psychiatrica Scandinavica 115, 104115.Google Scholar
Armitage, R, Hoffmann, R, Conroy, DA, Arnedt, JT and Brower, KJ (2012) Effects of a 3-hour sleep delay on sleep homeostasis in alcohol dependent adults. Sleep 35, 273278.Google Scholar
Armitage, R, Hoffmann, R, Fitch, T, Trivedi, M and Rush, AJ (2000) Temporal characteristics of delta activity during NREM sleep in depressed outpatients and healthy adults: group and sex effects. Sleep 23, 607617.Google Scholar
Armitage, R, Hoffmann, R, Trivedi, M and Rush, AJ (2000) Slow-wave activity in NREM sleep: sex and age effects in depressed outpatients and healthy controls. Psychiatry Research 95, 201213.Google Scholar
Baglioni, C, Nanovska, S, Regen, W, Spiegelhalder, K, Feige, B, Nissen, C, Reynolds, CF III and Riemann, D (2016) Sleep and mental disorders: a meta-analysis of polysomnographic research. Psychological Bulletin 142, 969990.Google Scholar
Beck, AT, Steer, RA and Brown, GK (1996) Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Borbely, AA (2001) From slow waves to sleep homeostasis: new perspectives. Archives Italiennes de Biologie 139, 5361.Google Scholar
Cheng, P, Goldschmied, J, Casement, M, Kim, HS, Hoffmann, R, Armitage, R and Deldin, P (2015) Reduction in delta activity predicted improved negative affect in Major Depressive Disorder. Psychiatry Research 228, 715718.Google Scholar
Curran, SL, Andrykowski, MA and Studts, JL (1995) Short form of the Profile of Mood States (POMS-SF): psychometric information. Psychological Assessment 7, 8083.Google Scholar
de Vivo, L, Bellesi, M, Marshall, W, Bushong, EA, Ellisman, MH, Tononi, G and Cirelli, C (2017) Ultrastructural evidence for synaptic scaling across the wake/sleep cycle. Science 355, 507510.Google Scholar
Diering, GH, Nirujogi, RS, Roth, RH, Worley, PF, Pandey, A and Huganir, RL (2017) Homer1a drives homeostatic scaling-down of excitatory synapses during sleep. Science 355, 511515.Google Scholar
Dinges, DF, Pack, F, Williams, K, Gillen, KA, Powell, JW, Ott, GE, Aptowicz, C and Pack, AI (1997) Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 20, 267277.Google Scholar
Drevets, WC, Price, JL, Simpson, JR Jr, Todd, RD, Reich, T, Vannier, M and Raichle, ME (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824827.Google Scholar
Duncan, WC, Sarasso, S, Ferrarelli, F, Selter, J, Riedner, BA, Hejazi, NS, Yuan, P, Brutsche, N, Manji, HK, Tononi, G and Zarate, CA (2013) Concomitant BDNF and sleep slow wave changes indicate ketamine-induced plasticity in major depressive disorder. The International Journal of Neuropsychopharmacology 16, 301311.Google Scholar
Gillin, JC, Buchsbaum, M, Wu, J, Clark, C and Bunney, W (2001) Sleep deprivation as a model experimental antidepressant treatment: findings from functional brain imaging. Depression and Anxiety 14, 3749.Google Scholar
Goldschmied, JR, Cheng, P, Armitage, R and Deldin, PJ (2014) Examining the effects of sleep delay on depressed males and females and healthy controls. Journal of Sleep Research 23, 664672.Google Scholar
Gorgulu, Y and Caliyurt, O (2009) Rapid antidepressant effects of sleep deprivation therapy correlates with serum BDNF changes in major depression. Brain Research Bulletin 80, 158162.Google Scholar
Kuhn, M, Wolf, E, Maier, JG, Mainberger, F, Feige, B, Schmid, H, Bürklin, J, Maywald, S, Mall, V and Jung, NH (2016) Sleep recalibrates homeostatic and associative synaptic plasticity in the human cortex. Nature Communications 7, 12455.Google Scholar
Kuhn, M, Mainberger, F, Feige, B, Maier, JG, Mall, V, Jung, NH, Reis, J, Kloppel, S, Normann, C and Nissen, C (2016) State-dependent partial occlusion of cortical LTP-like plasticity in major depression. Neuropsychopharmacology 41, 15211529.Google Scholar
Kupfer, DJ, Frank, E, McEachran, AB and Grochocinski, VJ (1990) Delta sleep ratio: a biological correlate of early recurrence in unipolar affective disorder. Archives of General Psychiatry 47, 11001105.Google Scholar
Landsness, EC, Goldstein, MR, Peterson, MJ, Tononi, G and Benca, RM (2011) Antidepressant effects of selective slow wave sleep deprivation in major depression: a high-density EEG investigation. Journal of Psychiatric Research 45, 10191026.Google Scholar
Lee, JH, Reynolds, CF, Hoch, CC, Buysse, DJ, Mazumdar, S, George, CJ and Kupfer, DJ (1993) Electoencephalographic sleep in recently remitted, elderly depressed patients in double-blind placebo-maintenance therapy. Neuropsychopharmacology 8, 143150.Google Scholar
Lindstrom, MJ and Bates, DM (1990) Nonlinear mixed effects models for repeated measures data. Biometrics 46, 673687Google Scholar
Liu, ZW, Faraguna, U, Cirelli, C, Tononi, G and Gao, XB (2010) Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 30, 86718675.Google Scholar
Lotrich, FE and Germain, A (2015) Decreased delta sleep ratio and elevated alpha power predict vulnerability to depression during interferon-alpha treatment. Acta Neuropsychiatrica 27, 1424.Google Scholar
McCormack, HM, David, JdL and Sheather, S (1988) Clinical applications of visual analogue scales: a critical review. Psychological Medicine 18, 10071019.Google Scholar
Nissen, C, Feige, B, König, A, Voderholzer, U, Berger, M and Riemann, D (2001) Delta sleep ratio as a predictor of sleep deprivation response in major depression. Journal of Psychiatric Research 35, 155163.Google Scholar
Nissen, C, Holz, J, Blechert, J, Feige, B, Riemann, D, Voderholzer, U and Normann, C (2010) Learning as a model for neural plasticity in major depression. Biological Psychiatry 68, 544552.Google Scholar
Pittenger, C and Duman, RS (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33, 88109.Google Scholar
Player, MJ, Taylor, JL, Weickert, CS, Alonzo, A, Sachdev, P, Martin, D, Mitchell, PB and Loo, CK (2013) Neuroplasticity in depressed individuals compared with healthy controls. Neuropsychopharmacology 38, 21012108.Google Scholar
Rechtschaffen, A and Kales, A (1968) A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. Los Angeles: BIS/BRI University of California.Google Scholar
Scott, JP, McNaughton, LR and Polman, RC (2006) Effects of sleep deprivation and exercise on cognitive, motor performance and mood. Physiology & Behavior 87, 396408.Google Scholar
Shacham, S (1983) A shortened version of the Profile of Mood States. Journal of Personality Assessment 47, 305306.Google Scholar
Swanson, LM, Hoffmann, R and Armitage, R (2010) Sleep macroarchitecture in depression: sex differences. The Open Sleep Journal 3, 1218.Google Scholar
Thase, ME, Fasiczka, AL, Berman, SR, Simons, AD and Reynolds, CF (1998) Electroencephalographic sleep profiles before and after cognitive behavior therapy of depression. Archives of General Psychiatry 55, 138144.Google Scholar
Tononi, G and Cirelli, C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Research Bulletin 62, 143150.Google Scholar
Tononi, G and Cirelli, C (2012) Time to be SHY? Some comments on sleep and synaptic homeostasis. Neural Plasticity 2012, 415250.Google Scholar
Watson, NF, Badr, MS, Belenky, G, Bliwise, DL, Buxton, OM, Buysse, D, Dinges, DF, Gangwisch, J, Grandner, MA and Kushida, C (2015) Recommended amount of sleep for a healthy adult: a joint consensus statement of the American Academy of Sleep Medicine and Sleep Research Society. Journal of Clinical Sleep Medicine 11, 591592.Google Scholar
Wirz-Justice, A, Van den, Hoofdakker and Rutger, H (1999) Sleep deprivation in depression: what do we know, where do we go? Biological Psychiatry 46, 445453.Google Scholar
Wolf, E, Kuhn, M, Normann, C, Mainberger, F, Maier, JG, Maywald, S, Bredl, A, Klöppel, S, Biber, K and van Calker, D (2016) Synaptic plasticity model of therapeutic sleep deprivation in major depression. Sleep Medicine Reviews 30, 5362.Google Scholar