Noise and the Brain. Experience Dependent Developmental and Adult Plasticity

385 Pages·2014·28.4 MB·English

by  Jos Eggermont (Auth.)

NOISE AND
THE BRAIN
NOISE AND
THE BRAIN
Experience Dependent
Developmental and
Adult Plasticity
J J. E
OS GGERMONT
EmeritusProfessorofPhysiology&Pharmacology,andPsychology
UniversityofCalgary
Calgary,Alberta,Canada
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Preface
Noise is more and more pervasive in modern society. While we are
slowly becoming aware of its potentially damaging consequences for
hearing, we should also appreciate the necessity of sound for normal
development of the auditory system and for keeping the central audi-
torysystemfinelytuned.Environmentalnoisehaslongbeenrecognized
as underlying psychosomatic problems such as sleeplessness, annoy-
ance, stress and hypertension. We are now in a position to trace the
brain structures involved in this process, which may lead to better
understanding of how these sounds affect us and how the effects can
be ameliorated. The emotional factors that distinguish our attitudes to
noise and music should also be put in perspective by elucidating the
good and bad parts of making music and listening to it. In this book I
bring together the varied types of sound and how they not only can
affect our hearing but also how they may promote maladaptive changes
in our brains, even in theabsence of hearing loss.
The topics in this book reflect the effects of different types of noise
(occupational, recreational, and environmental), and the noise levels,
which rangefromthosethatDON’Tresultindamagetotheeartothose
thatresultinpermanenthearingloss.Thesesoundshaveincommonthe
fact that they do affect auditory as well as nonauditory brain areas. The
auditory brain changes accompany perceptual changes in humans and
animals, whereas nonauditory brain areas are also involved in the psy-
chosomaticeffectsofnoise.Havingstudiedtheaspectsofnoiseonhear-
ing and deafness for more than four decades, I wanted to relate them to
their often co-occurring psychosomatic aspects. This required delving
into the psychological aspects of sound experiences, from pleasurable
(music)toannoying(environmentalnoise),andintosomaticreactionsto
sound ranging from the emotional (annoyance and stress) to the poten-
tially bodily harmful (sleeplessness and hypertension). I learned a lot
from studying this BOTH abundant and very specialized literature. In
thisbook,Iintegratethepsychosomaticeffectsofnoisewiththeirneuro-
physiological and pharmacological substrates in auditory and nonaudi-
tory brain areas. These substrates reflect the mechanisms that link
environmental noise to changes in emotion, stress and sleep that may
evenleadtocardiovascularproblems.
The composition of five chapters is to a large part driven by four
unexpected findings, two in animal research and two from human
ix
x
PREFACE
electrophysiology recordings. During my entire research career, I have
been fortunate to be able to combine basic animal and human research,
both on developmental aspects of hearing and on the consequences of
hearing loss and deafness in infancyand childhood.
Let’s start with the surprise findings in humans: when working on
auditory evoked potentials (AEP) in cochlear implant children some
unusual AEP waveform morphology was found and this prompted a
detailed investigation of the age-related changes in cortical auditory
evoked potentials in normal-hearing children. We (Curtis Ponton,
Manny Don, and I working at the House Ear Institute in Los Angeles)
found to our surprise that the morphology of the AEPs changed dra-
matically around 9(cid:1)11 years of age, from a dominant positive peaked
AEP to a dominant negative peaked AEP, and that the AEP properties
were not mature until the very late teens. We then looked again at the
results obtained in cochlear-implant patients. We found that their age-
dependent AEP properties following implantation were only compara-
ble with those of the controls when the age of the implanted child was
corrected by the duration of its deafness. Thus the “time-in-sound” or
“hearing age” was the determining factor for cortical maturation, illus-
trating that sound exposure is needed for normal development of the
auditory brain.Thesefindings take upthe majority ofChapters 4 and5.
In our animal experiments, we found unexpectedly that a moderate-
level sound, termed enhanced acoustic environment (EAE), applied for
three weeks immediately after an acoustic trauma, reduced the amount
of hearing loss compared to recovery in quiet. Furthermore, we found
the hypothesized abolishment of trauma-induced changes in cortical
tonotopic maps, in spontaneous firing rates, and in neural synchrony
found after recovery in quiet, although appreciable noise-induced hear-
ing loss remained. When applying this moderate level EAE exposure
for 5 months to normal hearing adult cats, basically a control study, we
found that the neurons in auditory cortex that normally would respond
to the frequency range of the EAE were now mostly unresponsive, but
that they fired strongly to sounds outside that frequency range.
This finding was reminiscent of the tonotopic-map reorganization in
auditory cortex that resulted from noise trauma. However, our cats
exposed to the EAE showed no hearing loss as measured by auditory
brainstem responses. This prompted a large parametric study on these
new effects of EAEs presented at levels B70dB SPL on the auditory
cortex. Thesefindings feature prominently inChapters 3, 4, and7.
These purely auditory chapters are put into broader perspective by
an introductory chapter covering early animal research on hearing and
hearing loss in the late 1800s and the first half of the 1900s, the discov-
ery that occupational noise exposure can be harmful to humans, and
the slow introduction of legislation to protect workers’ hearing from the
xi
PREFACE
effects of occupational noise. The second chapter covers some of the
important epidemiology and etiology of noise-induced hearing loss.
Here, I also introduce the reader to the fact that music making can be
considered a form of occupational noise and carries some of the same
harmful elements as industrial noise.
In Chapter 6 we cover the effects of background noise on speech, in
normalhearing,hearingimpairedandagingpeople.Basedonsomesem-
inalresearchinthe1970sand1980s,itbecomesclearthatlossofsensitiv-
ity barely explains the problems of hearing in the background of noise,
and points to effects of changes in the auditory brain itself. In Chapter 8
weexplorethecombinedeffectsofnoiseandaginguponthecochleaand
auditory brain. Whether the noise exposure is the cause of age-related
hearing impairment or contributes to it is explored in detail. Chapter 9
covers the good and bad aspects of music making and listening to loud
music.Thegoodaspectsofactivemusicmakingincludeenhancedcogni-
tive strengths, memory, and language ability, potentially identifying
music making as an antidote against the decreasing cognitive abilities
experiencedduringaging.Thebadaspectsarefullycomparabletothose
fromexposuretoloudoccupationalnoise.Theseharmfulresultsoccurin
classicalmusicians,popstarsanddiscjockeys,aswellasfromattending
loudconcertsandexcessivelisteningtoloudmusicfromMP3players.
Chapter10considersthenonauditoryaspectsofenvironmentalnoise.
I cover the brain pathways that lead from sound perception to annoy-
ance,stress,sleepproblemsandcardiovasculardisorders.Onthewayto
that sound(cid:1)brain network, some of the aspects of transportation noise
and wind-turbine sound that are important for brain-safe environments
are presented. One of the more troublesome effects of noise exposure is
tinnitus;thereforeIincludedChapter11on“noiseinthebrain,”andelu-
cidate that this internal noise can result in the same set of psychological
andpsychosomaticproblemsasenvironmentalnoise.Allthisculminates
in Chapter 12, which may be important for promoting general human
health in our current noisy environment. It does so by pointing to ways
forpreventing noise-inducedhearing loss,problemswithspeechunder-
standing,andarangeofpsychosomaticdisturbances.
I wish to thank my collaborators at the University of Calgary on this
project: Greg Shaw, Arnaud Noren˜a, Boris Goure´vitch, and Martin
Pienkowski, for feeding my interest in the effects of noise on and in the
brain.IalsowanttoextendmyappreciationtoCurtisPontonandManny
DonattheHouse-EarInstituteinLosAngelesforallowingmetotakepart
intheirexcitingresearch.ThankstomywifeMarywhoreadallthechap-
ters,withatranslator’sandauthor’seye,andcorrectedandshapedother-
wise unreadable sentences. I also want to thank April Graham, my
Editorial Project Manager at Academic Press, for prompt advice when I
neededit,andformakingwritingthisbookasmoothprocess.
Abbreviations
A1 primary auditory cortex
AAF anterior auditory field (cat)
ABR auditory brainstem response
ACC anterior cingulate cortex
ACh Acetylcholine
ACTH Adreno-CorticotropinHormone
AD adenosine
ADHD attention deficit and hyperactivity disorder
AEF auditory magnetic field
AEP auditory evoked potential
AF arcuatefasciculus
AI primary auditory cortex (cat)
AII secondaryauditorycortex (cat)
AIT auditory injury threshold, asymptoticthresholdshift
AM amplitude modulation
amHG anteromedialHeschl’s Gyrus
AMPA 2-amino-3-(3-hydroxy-5-methyl-isoxazol-4-yl)propanoic
acid
ANF auditory nerve fiber
ANS autonomous nervous system
ARHI age-related hearing impairment
ASSR auditory steady-state response
AVCN anterior part ofthe ventral cochlear nucleus
BA Brodmann area
BDNF brain-derived neurotrophic factor
BMF best modulation frequency
BOLD blood oxygen level(cid:1)dependent
CA conceptional age
cAMP Cyclicadenosine monophosphate
CAP compound action potential
CF characteristic frequency
ChAT Cholineacetyltransferase
CI confidence interval,also cochlearimplant
CN cochlearnucleus
CNS central nervous system
CP critical period
xiii
xiv
ABBREVIATIONS
CREB cyclicadenosinemonophospateresponseelementbinding
CRF corticotropin-releasing factor
CRH Corticotropin-releasing hormone
CS conditioned stimulus
CSD currentsource density
CSE cystathionine-c-lyase
CTL community tolerance level
dB decibel
dBA A-weighted average sound level
dBC C-weighted average sound level
DBP diastolicblood pressure
DCN dorsal cochlear nucleus
DENL day-evening-night level
DJ Disc jockey
DNL day-night level
DPOAE distortionproduct OAE
DTI diffusiontensor imaging
EABR electrically evokedABR
EAE enhancedacoustic environment
ECD equivalent currentdipole
EEG electroencephalography
ELAN early left anterior negativity
eMLR electrically evokedMLR
EPSP excitatory post-synaptic potentials
ER estrogenreceptor
ERAN early right anterior negativity
ERK extracellular signal-regulated kinase
ERP event relatedpotential
EU European Union
FFR frequency-following response
FGF Fibroblast growthfactor
FM frequency modulation
fMRI functional MRI
FS fast spiking
FTC frequency tuning curve
GABA gamma-aminobutyricacid
GAD glutamate decarboxylase
GAP growth-associated protein
GM gray matter
GR glucocorticoid receptor
GST Glutathione-S-transferase
HA hearing aid
HG Heschl’sgyrus
HL hearing level, alsohearing loss
xv
ABBREVIATIONS
HPA hypothalamic-pituitary-adrenal
HR hazardratio
HRP horse radishperoxidase
HSP heat-shock protein
Hz Herz
IC inferiorcolliculus
ICC central nucleus ofthe IC
ICMS intracortical microstimulation
IDT intensitydisciminationthreshold
IEG Immediate earlygene
IFG inferiorfrontal gyrus
IHC inner hair cell
IPSP inhibitory post-synapticpotentials
JNK c-Jun N-terminal kinase
kHz kilohertz
LA lateral nucleus of the amygdala
LC locus coeruleus
Lden see DENL
Ldn see DNL
LDT laterodorsal tegmentalnuclei
LFP local field potential
LOCB lateral olivocochlearbundle
LORETA low resolution brain electromagnetictomography
MAPK mitogen-activated protein kinase
MEG magnetoencephalogram
MGB medialgeniculate body
MGBm magnocellularpart of theMGB
MGBv ventral part of the MGB
MGN see MGB
MIHI music-induced hearing impairment
MLR middle-latency response
MMN mismatch negativity
MMR mismatch response
MP3 MovingPicture (Experts Group Code)3
MRI magnetic resonance imaging
MSO medialsuperiorolive
MSQ Mini SleepQuestionnaire
mtDNA mitochondrial DNA
MTF modulation transferfunction
MTG medialtemporal gyrus
MUA multi-unit activity
MW megaWatt
NAc nucleusacumbens
NAC N-acetylcysteine
xvi
ABBREVIATIONS
NHANES NationalHealth andNutritional Examination Surveys
NHCA NationalHearing Conservation Association
NICU neonatalintensive care unit
NIHL Noise-induced hearing loss
NIOSH NationalInstitute of Occupational Safety &Health
NMDA N-Methyl-D-aspartate
OAE oto-acoustic emission
OCB olivocochlear bundle
OHC outer hair cell
OR odds ratio
OSHA Occupational Safety and Health Administration
PC pyramidal cell
PCC posterior cingulated cortex
PCR polymerase chain reaction
PET positronemission tomography
PFC prefrontal cortex
PNE pulse-noise exposed
PNS parasympathetic nervoussystem
PPG DLpropargylglycine
PPI pre-pulseinhibition
PPT pedunculopontine tegmentalnuclei
PT planumtemporale
PTA pure-toneaverage
PTS permanent threshold shift
PVCN postero-ventral cochlear nucleus
PVN paraventricularnucleus
RAS reticularactivatingsystem
REM rapid eye movement
RMS root mean square
RNS reactive nitrogenspecies
ROI region of interest
ROS reactive oxygenspecies
RR relativerisk, seeHazard ratio
SBP systolic blood pressure
SD standarddeviation
SFR spontaneousfiring rate
SG spiral ganglion
SII speech intelligibilityindex
SLF superiorlongitudinal fasciculus
SNHL sensorineural hearing loss
SNP single nucleotidepolymorphism
SNR signal to noiseratio
SNS sympathetic nervous system
SOC superiorolivary complex