Chronic exposure to an environmental noise permanently disturbs sleep in rats: Inter-individual vulnerability

Chronic exposure to an environmental noise (EN) induces sleep disturbances. However, discrepancies exist in the literature since many contradictory conclusions have been reported. These disagreements are largely due to inappropriate evaluation of sleep and also to uncontrolled and confounding factors such as sex, age and also inter-individual vulnerability. Based on a recently validated animal model, aims of the present study were (i) to determine the effects of a chronic exposure to EN on sleep and (ii) to evaluate the inter-individual vulnerability of sleep to EN. For this purpose, rats were exposed during 9 days to EN. Results show that a chronic exposure to EN restricts continually amounts of slow wave sleep (SWS) and paradoxical sleep (PS) and fragments these two sleep stages with no habituation effect. Results also evidence the existence of subpopulations of rats that are either resistant or vulnerable to these deleterious effects of EN on sleep and especially on SWS amounts, bouts number and bout duration. Furthermore, importance of SWS debt and daily decrease of SWS bout duration are correlated to each others and both correlate to the amplitude of the locomotor reactivity to novelty, a behavioral measure of reactivity to stress. This last result suggests that this psychobiological profile of subjects, known to induce profound differences in neural and endocrine systems, could be responsible for their SWS vulnerability under a chronic EN exposure.

[1]  F. D. Hart,et al.  Waking performance decrements following minimal sleep disruption: The effects of habituation during sleep , 1975 .

[2]  Y. Wen,et al.  Repeated noise exposure affects muscarinic cholinergic receptors in the rat brain , 1989, Brain Research.

[3]  P. Piazza,et al.  Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration , 1991, Brain Research.

[4]  Daily sleep changes in a noisy environment assessed by subjective and polygraphic sleep parameters. , 1997 .

[5]  H Ising,et al.  Health effects caused by noise: evidence in the literature from the past 25 years. , 2004, Noise & health.

[6]  F. Fornai,et al.  Time-dependent changes in adrenal cortex ultrastructure and corticosterone levels after noise exposure in male rats. , 2001, European journal of morphology.

[7]  Shosuke Suzuki,et al.  HABITUATION OF SLEEP TO ROAD TRAFFIC NOISE AS DETERMINED BY POLYSOMNOGRAPHY AND AN ACCELEROMETER , 2001 .

[8]  A. Morrison,et al.  Increasing PGO spike density by auditory stimulation increases the duration and decreases the latency of rapid eye movement (REM) sleep , 1983, Brain Research.

[9]  Barbara Griefahn,et al.  Sleep Disturbances Related to Environmental Noise. , 2002, Noise & health.

[10]  G J Thiessen,et al.  Effect of continuous traffic noise on percentage of deep sleep, waking, and sleep latency. , 1983, The Journal of the Acoustical Society of America.

[11]  J. B. Justice,et al.  Response to novelty predicts the locomotor and nucleus accumbens dopamine response to cocaine , 1991, Synapse.

[12]  Shosuke Suzuki,et al.  Habituation of Sleep to a Ship's Noise as Determined by Actigraphy and a Sleep Questionnaire , 2002 .

[13]  H. Akil,et al.  Neurobiological Correlates of Individual Differences in Novelty-Seeking Behavior in the Rat: Differential Expression of Stress-Related Molecules , 2000, The Journal of Neuroscience.

[14]  J. Gabor,et al.  Sleep disruption in the intensive care unit , 2001, Current opinion in critical care.

[15]  M. Spreng,et al.  Ear damage caused by leisure noise. , 2001, Noise & health.

[16]  Shosuke Suzuki,et al.  DIFFERENT EFFECTS OF ROAD TRAFFIC NOISE AND FROGS' CROAKING ON NIGHT SLEEP , 2002 .

[17]  G. Labiale,et al.  LONG TERM SLEEP DISTURBANCE DUE TO TRAFFIC NOISE , 1983 .

[18]  M. Le Moal,et al.  Factors that predict individual vulnerability to amphetamine self-administration. , 1989, Science.

[19]  B. Jakovljević,et al.  Subjective reactions to traffic noise with regard to some personality traits , 1997 .

[20]  A. Giuditta,et al.  The Structure of Sleep is Related to the Learning Ability of Rats , 1993, The European journal of neuroscience.

[21]  D. Ouis Exposure to Nocturnal Road Traffic Noise: Sleep Disturbance and its After Effects. , 1999, Noise & health.

[22]  R T Wilkinson,et al.  Effects of traffic noise on quality of sleep: assessment by EEG, subjective report, or performance the next day. , 1984, The Journal of the Acoustical Society of America.

[23]  B. Griefahn,et al.  Noise and sleep at home, a field study on primary and after-effects , 1986 .

[24]  T J Balkin,et al.  Does sleep fragmentation impact recuperation?A review and reanalysis , 1999, Journal of sleep research.

[25]  Maria Casagrande,et al.  Auditory arousal thresholds after selective slow-wave sleep deprivation , 1999, Clinical Neurophysiology.

[26]  R. Job Community response to noise: A review of factors influencing the relationship between noise exposure and reaction , 1988 .

[27]  Shaul Feldman,et al.  Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli , 1995, Neuroscience & Biobehavioral Reviews.

[28]  R. Drucker-Colín,et al.  The effects of sensory stimulation on REM sleep duration. , 1998, Sleep.

[29]  P. Goldman-Rakic,et al.  Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism. , 1998, Archives of general psychiatry.

[30]  E. Oehrstroem EFFECTS OF LOW LEVELS OF ROAD TRAFFIC NOISE DURING THE NIGHT: A LABORATORY STUDY ON NUMBER OF EVENTS, MAXIMUM NOISE LEVELS AND NOISE SENSITIVITY , 1995 .

[31]  A. Rechtschaffen,et al.  Auditory Awakening Thresholds in Rem and Nrem Sleep Stages , 1966, Perceptual and motor skills.

[32]  C. Thiel,et al.  Auditory noise can prevent increased extracellular acetylcholine levels in the hippocampus in response to aversive stimulation , 2000, Brain Research.

[33]  R. Amici,et al.  Changes in REM sleep occurrence due to rhythmical auditory stimulation in the rat , 2000, Brain Research.

[34]  C. Sawyer,et al.  “Rebound” Recovery from Deprivation of Paradoxical Sleep in the Rabbit.∗ , 1963, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[35]  R. Drucker-Colín,et al.  The function of sleep is to regulate brain excitability in order to satisfy the requirements imposed by waking , 1995, Behavioural Brain Research.

[36]  Shosuke Suzuki,et al.  HABITUATION OF SLEEP TO ROAD TRAFFIC NOISE OBSERVED NOT BY POLYGRAPHY BUT BY PERCEPTION , 2002 .

[37]  D. Abrous,et al.  Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis , 1999, The European journal of neuroscience.

[38]  B. McEwen,et al.  Allostatic load: when protection gives way to damage. , 2003, Advances in mind-body medicine.

[39]  R. T. Wilkinson,et al.  Disturbance of sleep by noise: Individual differences , 1984 .

[40]  D. Dinges,et al.  Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. , 2004, Sleep.

[41]  Florian Holsboer,et al.  The Corticosteroid Receptor Hypothesis of Depression , 2000, Neuropsychopharmacology.

[42]  J. L. Eberhardt,et al.  The Disturbance by Road Traffic Noise of the Sleep of Young Male Adults as Recorded in the Home , 1987 .

[43]  M. Bonnet The effect of sleep fragmentation on sleep and performance in younger and older subjects , 1989, Neurobiology of Aging.

[44]  Henry Lai,et al.  Effects of noise on high-affinity choline uptake in the frontal cortex and hippocampus of the rat are blocked by intracerebroventricular injection of corticotropin-releasing factor antagonist , 1990, Brain Research.

[45]  B Griefahn A critical load for nocturnal high-density road traffic noise. , 1986, American journal of industrial medicine.

[46]  E. van Cauter,et al.  Sleep loss results in an elevation of cortisol levels the next evening. , 1997, Sleep.

[47]  M. Bonnet Auditory thresholds during continuing sleep , 1986, Biological Psychology.

[48]  J. P. Huston,et al.  High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessments , 1999, Neuroscience.

[49]  M. Opp,et al.  Role of corticotropin-releasing hormone in stressor-induced alterations of sleep in rat. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[50]  Shosuke Suzuki,et al.  TRANSIENT EFFECT OF THE NOISE OF PASSING TRUCKS ON SLEEP EEG , 1997 .

[51]  M. Le Moal,et al.  Novelty-seeking in rats--biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. , 1996, Neuropsychobiology.

[52]  H. Ising,et al.  Acute and chronic endocrine effects of noise: Review of the research conducted at the Institute for Water, Soil and Air Hygiene. , 2000, Noise & health.

[53]  N. Carter Transportation noise, sleep, and possible after-effects , 1996 .

[54]  R. Job Noise sensitivity as a factor influencing human reaction to noise. , 1999, Noise & health.

[55]  M. Le Moal,et al.  Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. , 1996, Annual review of pharmacology and toxicology.

[56]  R.F.S. Job,et al.  The influence of subjective reactions to noise on health effects of the noise , 1996 .

[57]  G. Thiessen,et al.  Effect of intermittent truck noise on percentage of deep sleep. , 1978, The Journal of the Acoustical Society of America.

[58]  J. Aran,et al.  Deleterious effects of an environmental noise on sleep and contribution of its physical components in a rat model , 2004, Brain Research.

[59]  W. Babisch The Noise/Stress Concept, Risk Assessment and Research Needs. , 2002, Noise & health.

[60]  Evy Öhrström,et al.  SLEEP DISTURBANCE EFFECTS OF TRAFFIC NOISE--A LABORATORY STUDY ON AFTER EFFECTS , 1982 .

[61]  L A Reyner,et al.  A field study of sleep disturbance: effects of aircraft noise and other factors on 5,742 nights of actimetrically monitored sleep in a large subject sample. , 1994, Sleep.

[62]  M. Terzano,et al.  Modifications of sleep structure induced by increasing levels of acoustic perturbation in normal subjects. , 1990, Electroencephalography and clinical neurophysiology.

[63]  G. Housley,et al.  Noise exposure induces up-regulation of ecto-nucleoside triphosphate diphosphohydrolases 1 and 2 in rat cochlea , 2004, Neuroscience.