Effects of sleep deprivation on central auditory processing

BMC Neuroscience

Ari Leon Jurkiewicz³  Jair Mendes Marques³  Bianca Simone Zeigelboim³  Mara L Cordeiro²  Karlin Fabianne Klagenberg D’Andrea³  Paulo Breno Noronha Liberalesso¹ 

[1] Department of Neuropediatrics, Little Prince Children’s Hospital, Curitiba, Brazil;Department of Psychiatry and Biobehavioral Sciences of the David Geffen School of Medicine, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, USA;University Tuiuti of Paraná, Otoneurology Research Center, Curitiba, Brazil

关键词: SSWT;    RGDT;    Sleep;    Central auditory processing;   

Others  :  1170632
DOI  :  10.1186/1471-2202-13-83

 received in 2012-02-08, accepted in 2012-07-23,  发布年份 2012

【 摘 要 】

Background

Sleep deprivation is extremely common in contemporary society, and is considered to be a frequent cause of behavioral disorders, mood, alertness, and cognitive performance. Although the impacts of sleep deprivation have been studied extensively in various experimental paradigms, very few studies have addressed the impact of sleep deprivation on central auditory processing (CAP). Therefore, we examined the impact of sleep deprivation on CAP, for which there is sparse information. In the present study, thirty healthy adult volunteers (17 females and 13 males, aged 30.75 ± 7.14 years) were subjected to a pure tone audiometry test, a speech recognition threshold test, a speech recognition task, the Staggered Spondaic Word Test (SSWT), and the Random Gap Detection Test (RGDT). Baseline (BSL) performance was compared to performance after 24 hours of being sleep deprived (24hSD) using the Student’s t test.

Results

Mean RGDT score was elevated in the 24hSD condition (8.0 ± 2.9 ms) relative to the BSL condition for the whole cohort (6.4 ± 2.8 ms; p = 0.0005), for males (p = 0.0066), and for females (p = 0.0208). Sleep deprivation reduced SSWT scores for the whole cohort in both ears [(right: BSL, 98.4 % ± 1.8 % vs. SD, 94.2 % ± 6.3 %. p = 0.0005)(left: BSL, 96.7 % ± 3.1 % vs. SD, 92.1 % ± 6.1 %, p < 0.0001)]. These effects were evident within both gender subgroups [(right: males, p = 0.0080; females, p = 0.0143)(left: males, p = 0.0076; females: p = 0.0010).

Conclusion

Sleep deprivation impairs RGDT and SSWT performance. These findings confirm that sleep deprivation has central effects that may impair performance in other areas of life.

【 授权许可】

   
2012 Liberalesso et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Chokroverty S: Overview of sleep & sleep disorders. Indian J Med Res 2010, 131:126-140.
• [2]Stickgold R, Hobson JA, Fosse R, Fosse M: Sleep, learning, and dreams: off-line memory reprocessing. Science 2001, 294(5544):1052-1057.
• [3]Stickgold R, Walker MP: Sleep-dependent memory consolidation and reconsolidation. Sleep Med 2007, 8(4):331-343.
• [4]Bonnet MH, Arand DL: We are chronically sleep deprived. Sleep 1995, 18(10):908-911.
• [5]Levine B, Lumley M, Roehrs T, Zorick F, Roth T: The effects of acute sleep restriction and extension on sleep efficiency. Int J Neurosci 1988, 43(3–4):139-143.
• [6]Imeri L, Opp MR: How (and why) the immune system makes us sleep. Nat Rev Neurosci 2009, 10(3):199-210.
• [7]Robillard R, Lanfranchi PA, Prince F, Filipini D, Carrier J: Sleep deprivation increases blood pressure in healthy normotensive elderly and attenuates the blood pressure response to orthostatic challenge. Sleep 2011, 34(3):335-339.
• [8]Silva JA, Costa E: Sleep disorders in psychiatry. Metabolism 2006, 55(10 Suppl 2):S40-S44.
• [9]Kyung Lee E, Douglass AB: Sleep in psychiatric disorders: where are we now? Can J Psychiatry 2010, 55(7):403-412.
• [10]Mirescu C, Peters JD, Noiman L, Gould E: Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc Natl Acad Sci USA 2006, 103(50):19170-19175.
• [11]Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Wong C, Ma J, Pradhan K, Tomasi D, Thanos PK, et al.: Sleep deprivation decreases binding of [11 C]raclopride to dopamine D2/D3 receptors in the human brain. J Neurosci 2008, 28(34):8454-8461.
• [12]Friederici AD: Towards a neural basis of auditory sentence processing. Trends Cogn Sci 2002, 6(2):78-84.
• [13]Harrison Y, Horne JA: The impact of sleep deprivation on decision making: a review. J Exp Psychol Appl 2000, 6(3):236-249.
• [14]Harrison Y, Horne JA: Sleep loss and temporal memory. Q J Exp Psychol A 2000, 53(1):271-279.
• [15]Babkoff H, Zukerman G, Fostick L, Ben-Artzi E: Effect of the diurnal rhythm and 24 h of sleep deprivation on dichotic temporal order judgment. J Sleep Res 2005, 14(1):7-15.
• [16]Katz J, Smith PS: The Staggered Spondaic Word Test A ten-minute look at the central nervous system through the ears. Ann N Y Acad Sci 1991, 620:233-251.
• [17]Harrison Y, Horne JA, Rothwell A: Prefrontal neuropsychological effects of sleep deprivation in young adults–a model for healthy aging? Sleep 2000, 23(8):1067-1073.
• [18]Tomasi D, Wang RL, Telang F, Boronikolas V, Jayne MC, Wang GJ, Fowler JS, Volkow ND: Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 2009, 19(1):233-240.
• [19]: Randon Gap Detection Test. . [www.auditec.com webcite]
• [20]Keith RW, Katbamna B, Tawfik S, Smolak LH: The effect of linguistic background on staggered spondaic word and dichotic consonant vowel scores. Br J Audiol 1987, 21(1):21-26.
• [21]Palfery TD, Duff D: Central auditory processing disorders: review and case study. Axone 2007, 28(3):20-23.
• [22]Paavonen EJ, Raikkonen K, Pesonen AK, Lahti J, Komsi N, Heinonen K, Jarvenpaa AL, Strandberg T, Kajantie E, Porkka-Heiskanen T: Sleep quality and cognitive performance in 8-year-old children. Sleep Med 2010, 11(4):386-392.
• [23]Ayalon L, Ancoli-Israel S, Klemfuss Z, Shalauta MD, Drummond SP: Increased brain activation during verbal learning in obstructive sleep apnea. NeuroImage 2006, 31(4):1817-1825.
• [24]Beebe DW, Rose D, Amin R: Attention, learning, and arousal of experimentally sleep-restricted adolescents in a simulated classroom. J Adolesc Health 2010, 47(5):523-525.
• [25]Chee MW, Choo WC: Functional imaging of working memory after 24 hr of total sleep deprivation. J Neurosci 2004, 24(19):4560-4567.
• [26]Pilcher JJ, Band D, Odle-Dusseau HN, Muth ER: Human performance under sustained operations and acute sleep deprivation conditions: toward a model of controlled attention. Aviat Space Environ Med 2007, 78(5 Suppl):B15-B24.
• [27]Adam M, Retey JV, Khatami R, Landolt HP: Age-related changes in the time course of vigilant attention during 40 hours without sleep in men. Sleep 2006, 29(1):55-57.
• [28]Tucker AM, Whitney P, Belenky G, Hinson JM, Van Dongen HP: Effects of sleep deprivation on dissociated components of executive functioning. Sleep 2010, 33(1):47-57.
• [29]Libedinsky C, Smith DV, Teng CS, Namburi P, Chen VW, Huettel SA, Chee MW: Sleep deprivation alters valuation signals in the ventromedial prefrontal cortex. Front Behav Neurosci 2011, 5:70.
• [30]Boutrel B, Koob GF: What keeps us awake: the neuropharmacology of stimulants and wakefulness-promoting medications. Sleep 2004, 27(6):1181-1194.
• [31]Andersen ML, Martins PJ, D'Almeida V, Bignotto M, Tufik S: Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J Sleep Res 2005, 14(1):83-90.
• [32]Martins RC, Andersen ML, Garbuio SA, Bittencourt LR, Guindalini C, Shih MC, Hoexter MQ, Bressan RA, Castiglioni ML, Tufik S: Dopamine transporter regulation during four nights of REM sleep deprivation followed by recovery–an in vivo molecular imaging study in humans. Sleep 2010, 33(2):243-251.
• [33]Barkley RA, Grodzinsky G, DuPaul GJ: Frontal lobe functions in attention deficit disorder with and without hyperactivity: a review and research report. J Abnorm Child Psychol 1992, 20(2):163-188.
• [34]Brennan AR, Arnsten AF: Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann N Y Acad Sci 2008, 1129:236-245.
• [35]Petersen SE, Posner MI: The attention system of the human brain: 20 years after. Annu Rev Neurosci 2012, 35:73-89.
• [36]Wu JC, Gillin JC, Buchsbaum MS, Chen P, Keator DB, Khosla Wu N, Darnall LA, Fallon JH, Bunney WE: Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 2006, 31(12):2783-2792.
• [37]Quintas VG, Attoni TM, Keske-Soares M, Mezzomo CL: Auditory processing and phonological awareness in children with normal and deviant speech development. Pro Fono 2010, 22(4):497-502.
• [38]Steenari MR, Vuontela V, Paavonen EJ, Carlson S, Fjallberg M, Aronen E: Working memory and sleep in 6- to 13-year-old schoolchildren. J Am Acad Child Adolesc Psychiatry 2003, 42(1):85-92.
• [39]Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M, Huang T, Brown KM, Li XY, Descalzi G, et al.: Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 2009, 461(7267):1122-1125.
• [40]Samelli AG, Schochat E: The Gap-in-noise test: gap detection thresholds in normal hearin young adults. Int J Audiol 2008, 47(5):238-245.
• [41]Killgore WD: Effects of sleep deprivation on cognition. Prog Brain Res 2010, 185:105-129.
• [42]Kopasz M, Loessl B, Valerius G, Koenig E, Matthaeas N, Hornyak M, Kloepfer C, Nissen C, Riemann D, Voderholzer U: No persisting effect of partial sleep curtailment on cognitive performance and declarative memory recall in adolescents. J Sleep Res 2010, 19(1 Pt 1):71-79.
• [43]Brun CC, Lepore N, Luders E, Chou YY, Madsen SK, Toga AW, Thompson PM: Sex differences in brain structure in auditory and cingulate regions. Neuroreport 2009, 20(10):930-935.
• [44]Shively CA, Bethea CL: Cognition, mood disorders, and sex hormones. ILAR J 2004, 45(2):189-199.
• [45]Wallentin M: Putative sex differences in verbal abilities and language cortex: a critical review. Brain Lang 2009, 108(3):175-183.
• [46]Dinges DF, Pack F, Williams K, Gillen KA, Powell JW, Ott GE, Aptowicz C, Pack AI: Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 1997, 20(4):267-277.
• [47]Lim J, Dinges DF: Sleep deprivation and vigilant attention. Ann N Y Acad Sci 2008, 1129:305-322.