Noise and the Brain: Experience Dependent Developmental and Adult Plasticity

1

Introduction

Noise affects the brain in many ways. The most obvious one is by causing hearing loss, which in turn results in changes in the brain that can result in tinnitus. Only in the early 19th century were occupational hazards resulting in deafness identified. Animal studies in the early 20th century discovered the neural substrates thereof, and safe exposure levels were established. More recently, it has been demonstrated that even legally safe noise exposure levels, if presented for a long time, can cause long-lasting changes in the central auditory nervous system, in the absence of demonstrable hearing loss. Recreational noise, such as loud music, currently competes with occupational noise exposure for being a primary cause of hearing impairment. Environmental noise can, beyond being a source of annoyance, also cause sleep problems and stress. This introductory chapter uses a historical approach to this manifold of effects of noise on the brain, and concludes that prevention is the best solution.

Keywords

History; Deafness; Neural substrates; Safe exposure levels; Tonotopic maps; Brain plasticity; Noise annoyance; Noise prevention

Ten thousand years ago, the world must have been a quiet place. But already a few thousand years ago there were busy markets and workplaces of blacksmiths and other artisans. And by that time¹ occupational noise problems such as tinnitus had been noted. In contrast to antiquity, ours is a world of excessive exposure to sound resulting from a variety of occupational, environmental, and recreational sources. The most important aspect in this deterioration of environmental and occupational acoustical conditions is without a doubt the industrial revolution (1750–1850). Environmental sound levels now generally exceed 80 dBA (Figure 1.1).

Figure 1.1 Filter curves (weightings) for sound level measurements (left). The filter gain is plotted as a function of sound frequency on double logarithmic scales. Sound levels with indications of sources and approximate loudness (right). A-weighting (blue) is the most commonly used of a family of curves defined in the International standard IEC 61672:2003 for the measurement of sound levels. The integrated energy below the weighting curve is typically indicated as dBA. A-weighting, which is basically the inverse of the human threshold as a function of frequency, is mandated for the measurement of environmental noise and industrial noise, as well as when assessing potential hearing damage and other noise health effects at all sound levels. For measuring low frequency (infra) sounds the C-weighting (red) is better. The B and D weightings are hardly ever used. Modified from Wikipedia (2011).

According to the World Health Organization’s Guidelines for Community Noise,² noise can result in adverse health effects such as: hearing loss, sleep disturbances, and even cardiovascular problems. In addition, environmental sound may cause behavioral problems such as reduced performance, annoyance reactions, and even adverse social behavior.

Sound may be annoying noise or may be music to our ears; however, for some people music can also be annoying. Recently, more people have become aware of the potential damage that excessive sound (noise as well as music) exposure may cause to our hearing. Whereas there are fairly stringent occupational noise standards to protect workers’ hearing sensitivity, very few people are currently aware of the effects that continuous or interrupted (e.g., day–night) occupational or environmental long-term exposure to non-hearing–loss-causing sound can inflict on the body and brain. In addition to the effects listed in the first paragraph, it is becoming more and more obvious that sounds that do not cover the entire audible frequency range create the most problems.³ These sounds result in long-lasting downregulation of the neural gain in the auditory system over the exposure-sound frequency range combined with an upregulation of the gain in nonexposed frequency regions. This can, for instance, result in differential amplification of vowels and consonants. This is known to be at the source of reduced speech understanding.⁴

Sometimes these frequency-dependent gain-change effects are seen as beneficial. For instance, people who live along a busy street often say that they are no longer aware of the traffic noise. The psychological explanation is that they have habituated to it. Habituation to sound is an example of nonassociative learning that is based on reduced neural activity in the central auditory system and is specific to that particular type of sound. The reduced neural activity in response to such behaviorally meaningless sound may also help in perceiving other meaningful sounds.⁵ Common experience indicates that the city dweller, frequently encountering significant levels of outdoor and indoor noise, becomes accustomed to such exposures and can sleep in their presence. I personally experienced this while staying in Bilbao, Spain, during the festive week of Asta Nagusta 2012 featuring a drone of loud music and noisy revelers during the entire, and every, night on the square bordering my hotel. The first few nights I hardly could sleep, but the remainder of the week showed great improvement in that respect. However, specifically traffic noise appears hard to habituate to and causes alterations in subjective evaluation of sleep, annoyance, and work performance.⁶ Exposure to environmental sound is one of the many factors that contribute to noise annoyance. Noise annoyance is generally characterized as a feeling of resentment, displeasure, discomfort, dissatisfaction, or offense when noise interferes with someone’s thoughts, feelings, or actual activities.⁷ An important question is whether the brain changes that underlie habituation to particular sounds also affect the perception of other sounds. That is not clear and depends on how well habituation as currently defined explains these brain changes. What is known is that long-term exposure to noise (not necessarily damaging) impairs sound processing in auditory cortex as well as attention.⁸

The neuroscience aspects of the problems that I want to address in this book in particular are, first, the effects of traumatic noise leading to hearing loss and the subsequent changes in the auditory brain. Secondly, and perhaps more importantly, I will address our recent discovery that even moderate level sound exposure (long duration continuous or periodic—day/night) also has long-lasting effects on the adult brain without causing audiometric hearing loss. This happens even more so in neonates, infants and children, and thus is a life-span problem. The ultimate effects of such exposures may be similar in all age groups, but they are induced faster and leave permanent changes in a neonatal and infant brain. In contrast, these changes are induced slower and are up to a point spontaneously but slowly reversible in adult brains. The sounds that induce these changes are generally behaviorally irrelevant—i.e., do not require any behavioral actions. Sound without behavioral meaning is colloquially described as noise. In real life this can be occupational, recreational, environmental or, if loud enough, so-called traumatic noise. Loud noise above the occupational-noise exposure limits can damage the cochlea, causes hearing loss, and as a consequence also induces changes in the brain. Long-term exposure to moderate-level noise can also result in dramatic frequency-dependent changes in cortical neural sensitivity without causing hearing sensitivity loss. Besides these neuronal changes in the auditory brain, noise exposure can also cause sleep disturbances resulting in stress, hypertension and potentially cardiovascular problems, and thus in the long term affects both brain and nonbrain systems. The sound-to-brain interface that causes these bodily changes is becoming better defined. We will explore these findings in Chapters 10 and 11. Still, sound is required for normal auditory brain development.⁹ Powerful electric prostheses (cochlear implants) can restore sound perception to such an extent that normal conversation is possible. We will explore the effects thereof on the brain in Chapter 5.

1.1 Discovery of Noise as a Cause of Hearing Loss

In addition to being a statesman, Sir Francis Bacon (1561–1626) wrote essays on hearing speech and sound. These are included in his book Sylva Sylvaram: Or a naturall historie in ten centuries.¹⁰ He describes therein his experience with a temporary hearing threshold shift and transient tinnitus:

A very great sound, neere hand, hath strucken many Deafe; And at the Instant they have found, as it were, the breaking of a Skin or Parchment in their Eare: And my selfe standing neere on that Lured loud, and shrill, had suddenly an Offence, as if somewhat had broken, or beene dislocated in my Eare; And immediately after, a loud Ringing; (Not an ordinary Singing, or Hissing, but farre louder, and differing;) so as I feared some Deafenesse. But after some halfe Quarter of an Houre it vanished.

Two hundred years later, Fosbroke¹¹ provided a quite comprehensive account of the etiology of hearing loss. He distinguished between traumatic deafness following the sudden explosion of a cannon, and deafness caused by occupational noise, e.g., blacksmith’s deafness. He reported two cases of traumatic deafness, that of Lord Rodney after the eighty broadsides fired from his ship the Formidable, in 1782, and a second from the report of a cannon close to the individual at the battle of Copenhagen. He then describes the deafness suffered by blacksmiths as being (cited in¹²):

… a consequence of their employment; it creeps on them gradually, in general at about forty or fifty years of age. At first the patient is insensible of weak impressions of sound; the deafness increases with a ringing and noise in the ears, slight vertigo, and pain in the cranial bones, periodical or otherwise, and often violent. No wax is formed. It has been imputed to a paralytic state of the nerve, occasioned by the noise of forging, by certain modem writers, and by the old writers, to permanent over-tension of the membrane, which they compare to fixed dilatation of the pupil.

Systematic studies in occupational deafness were also emerging in the late 1800s. The studies by Gottstein and Kayser in Germany, and by Barr in Scotland, were identified by Atherley and Noble¹² as the two principal landmarks representing research in this time period. I follow their extensive review. Gottstein and Kayser¹³ were the first to perform a controlled study by comparing the hearing of an experimental group, comprising blacksmiths and metal workers, with that of a control group consisting of bricklayers. They assigned good, fairly bad and bad hearing to those who could hear whispered speech beyond 3 m, those who could hear it only at a distance of 2–3 m, and those who could hear it only when presented close to the ear or not at all. Note that whispered speech contains mostly high frequencies, and that this test does not assess residual low-frequency hearing. They found increasing hearing loss with age in the blacksmiths: none over the age of 50 could hear well and those that were older presented nearly total loss of hearing. By contrast, only two of the 36 bricklayers were in the fairly bad or bad categories.

Barr’s¹⁴ main testing equipment was his pocket watch. He reported this being heard when the hearing is normal 36 inches from the ear. How the distance for normal hearing was arrived at Barr does not say, but it was likely determined by holding his watch at arms-length; 36 inches equals one yard. Barr used his watch to test the hearing of 100 men working as boilermakers in two Glasgow shipyards. He characterized them as follows:

The 100 men examined represent all ages, from 17 years, the youngest, to 67, the oldest. The average age was 35. The most serious results were found, as might have been expected, in the older men. The average number of years during which they had been exposed to the sounds of boiler making was 17½; the oldest had been at the trade for 54 years, and the youngest for three years.

Barr also took up the cause of those with hearing impairment, estimating their prevalence as 10% of the adult population (see Chapter 2 for similar contemporary results). He pleaded for better acoustical design of public meeting places, and closer concern by clergy and other public speakers over the clarity of delivery of their message. He also appealed to them to refrain from growing bushy beards and moustaches (so as to allow lip reading). Finally, Barr devoted considerable and careful attention to hearing-protection devices, such as India-rubber plugs and cotton plugs smeared with Vaseline. He warned about problems with fitting earplugs, of irritation of the meatus, and the potential lack of motivation to use such devices among industrial workers. All in all, his advice represents a modern perspective indeed.

Experimental studies into the etiology of occupational hearing loss started to emerge at the beginning of the 20th century. Rodger,¹⁵ who was a clinical assistant from the Ear and Throat Department of the Royal Infirmary of Edinburgh, wrote:

… such a wealth of laboratory results having thus recently been placed at our disposal, there is room for further clinical investigation, to extend the observations of Barr and Habermann already referred to, and I now propose to submit some notes on the examination of forty-eight cases of occupation deafness. Of these, four were seen in Dr. Logan Turner’s clinic, two being blacksmiths, one an engineer, and one a brass-finisher. The remaining forty-four were boiler-makers and rivetters, who were seen, not as patients, but for the purpose of the investigation. Care was taken to secure a proper proportion of the younger men, so that the condition might be studied in relation to the length of time the trade had been engaged in.

Rodger’s conclusions are remarkably prescient¹⁵:

(1) That loss of hearing for high notes is not, as hitherto taught, the outstanding feature of noise-deafness. (2) That the predominant noises to which the patient has been exposed determine the site of the initial lesion in the inner ear, and that for a considerable time the depreciation of hearing is mainly for sounds of a pitch corresponding to these noises. (3) That later, the unusual vulnerability of the lowest part of the cochlear canal gives rise to marked loss of hearing for high tones. (4) That the vestibular apparatus in such occupations as boilermaking, where loud hammering is being carried on, is also affected, although in less degree than the cochlear apparatus. (5) That the condition of noise-deafness could be to a very large extent obviated by the use of suitable ear-plugs.

Quantification of hearing loss followed the introduction of the audiometer; early electro-mechanical versions of which were those by Hartmann¹⁶ and Hughes.¹⁷ Electronic developments during World War I led to the introduction of electronic-valve based audiometers. The first commercially available one, the Weston Electric 1A audiometer, was among others developed by Fowler who was also one of the first to report their use.¹⁸ Fowler,¹⁹ in a presentation before the American Otological Society under the title, Marked Deafened Areas in Normal Ears, commented on the frequent appearance of tonal gaps in hearing sensitivity:

One striking phenomenon seen in a large percentage of hearing graphs is a marked dip in the curve between 1,000 and 5,000 cycles (most often about 3,000 or 4,000). This occurs frequently in both normal and abnormal ears.

A year later, Fowler concluded that normal ears (as redefined compared to his earlier study) did not show these gaps and discussed the possibility of these gaps resulting from acoustic trauma. He stated²⁰:

It would appear that mid-high frequencies were particularly sensitive to various insults, especially acoustic trauma and toxic neuritis, because they regularly fail to escape in these conditions…. It would appear that there is an element of toxic neuritis or trauma diagnosable by the presence of marked deafened areas (dips) and otherwise unascertainable.

It is remarkable that clinical audiometry has not substantially evolved in the last half of the 20th century beyond the use described by Fowler. For research purposes, into the early aspects of noise trauma, the high-frequency limit has only occasionally been extended to 16 kHz.

Mechanical hearing aids also started to be used in the early 19th century. Mills²¹ in her review on electronic hearing aids phrased it as follows:

The first dedicated hearing aid firm, Frederick Rein of London, began to manufacture ear trumpets, hearing fans, and conversation tubes in 1800. Trumpets and tubes ‘amplified’ by collecting and concentrating sound waves that would otherwise disperse. As such, their design was an ongoing compromise between amplification and portability—the longer the trumpet and the wider its bell, the greater the magnification of sound.

1.2 Experimental Studies in Animals and the Establishment of the Neural Substrates of Hearing

1.2.1 Early Theories of Hearing

At the time of the earliest animal studies of hearing and hearing loss, researchers entertained two main theories of hearing that were arrived at on basis of human psychoacoustic studies: one from Helmholtz that assumed that pitch was related to the place of activation in the cochlea²² and the other, espoused by Wundt, that pitch was related to the periodicity in the firing of auditory nerve fibers.²³ It is interesting to note that Wundt was a student of Helmholtz and Müller. Müller²⁴ proposed the doctrine of specific energies of the different senses, which states that stimulating a fiber of the optical nerve always results in a visual sensation, stimulating a fiber of the acoustical nerve in an auditory sensation, etc.

Helmholtz’s hearing theory was based on two hypotheses. First, that the analysis of sound is accomplished in the inner ear by means of a large number of resonators tuned to different frequencies from low to high, low corresponding to the apical end and high to the basal end of the basilar membrane. This is the physiological counterpart of the view that the frequency-analyzing power of the ear is analogous to Fourier analysis of periodic functions as was proposed by Ohm.²⁵ On the basis of psychoacoustic evidence, Helmholtz estimated the sharpness of the resonators as having a bandwidth of 4% of the resonance frequency, and thus be proportional to frequency. Helmholtz also assumed that the local vibrations of the basilar membrane in the cochlea gave rise to activity of corresponding nerve fibers in the organ of Corti. The organ of Corti (or spiral organ) is the organ in the mammalian inner ear that contains the auditory sensory cells, or hair cells. The organ was named after the Italian anatomist Corti (1822–1876), who conducted microscopic research of the mammalian auditory system. This led to Helmholtz’s second hypothesis: A specific pitch corresponds to each of the nerve fibers that contact the hair cells in the organ of Corti in such a way that pitch decreases gradually from the basal to the apical end of the basilar membrane. This hypothesis can be considered as an extension of Müller’s²⁴ theory of specific energies. Helmholtz’s theory became widely accepted soon under the names of resonance theory or place theory of hearing. It correlates frequency with place (Hypothesis 1) and place with pitch (Hypothesis 2), so it assumes a frequency–pitch correspondence.²⁶

Wundt²³ proposed an alternative explanation of pitch, interestingly based on physiological investigations by Helmholtz that were unrelated to the auditory system. Helmholtz²⁷ had found that stimulating muscles via their nerves with periodic electric pulses gave rise to synchronous mechanical vibrations of the muscle. Up to stimulation with about 240 pulses-per-second, these vibrations manifested themselves by a clear tone emitted from the muscle. In the second edition of his work Grundzuge der Physiologischen Psychologie Wundt criticized Helmholtz’s second hypothesis that cochlear place is correlated with pitch. While accepting his first hypothesis that different locations along the basilar membrane are tuned to different frequencies, Wundt proposed an alternative for Helmholtz’s second hypothesis: Tones give rise to synchronous nerve impulses whose rate determines pitch. The pitch perception theory promoted by Wundt assumed a periodicity–pitch correspondence. Although Wundt’s theory could explain some observations with complex sounds much better than the resonance theory, its influence was much smaller than that of Helmholtz.²⁶ Wundt’s theory was resurrected by his student Wever (see below) and evolved in the Volley Theory of hearing.²⁸

1.2.2 Experimental Tests in Animals

The first experimental studies on noise-induced deafness were likely conducted by Wittmaack²⁹ in Germany and Yoshii³⁰ in Switzerland. Whereas Wittmaack did not find frequency-specific lesions in the cochlea, which would favor a place theory of pitch, Yoshii did (citation from¹⁵):

With a whistle producing a note=C⁵ (about 4096 double vibrations per second) Yoshii found the maximum amount of atrophy consistently located in the upper half of the basal coil of the cochlea; one producing a note=A² (about 838 double vibrations) gave changes in the middle and upper part of the second lowest coil; while one producing a note=G (about 192 double vibrations) gave rise to changes half a coil higher. It was found that, no matter how pure the note was, the pathological change had quite a measurable distribution, being most marked in the centre of the area involved and tapering off above and below. Yoshii accordingly assumes that Helmholtz’s theory is essentially correct, although the parts of the sound-perceiving endorgan are not so definitely isolated in their action as the parts of the keyboard of a musical instrument.

Prior to further investigations on the neural substrate of hearing, animal behavioral experiments related to hearing and deafness were carried out. Sir Francis Galton often carried on the end of his walking stick one of those small silent dog-whistles now known by his name, and tested the animals he encountered by sounding a shrill note and observing whether the animal seemed to respond. This was the same Galton that created the statistical concept of correlation and was the first to apply statistical methods to the study of human differences and inheritance of intelligence, and introduced the use of questionnaires and surveys for collecting such data. Using his whistle, Galton³¹ found that cats have the most all-round sensitive hearing, being able from a considerable distance to hear notes too high in frequency for humans to hear, and small dogs can also hear these notes, while large dogs cannot. However, nearly half a century later Upton³² still remarked that:

There has been considerable investigation of hearing in the higher vertebrates and, in spite of some very favorable evidence, the general impression seems to be that many of the mammals are able to hear noises but are deaf to tones.

Upton subsequently directed his efforts at how to destroy the hearing ability in guinea pigs, which led him to state that³³:

1) Exposure to an intense tone over an extended period of time is accompanied by the appearance of definite functional changes in the responses of guinea pigs to auditory stimuli: a) There is a total loss of sensitivity to tones of the exposure frequency within a very wide range of intensities. A low degree of sensitivity to very high intensities of the exposure frequency remains after the period of exposure. b) When the exposure tone is of lower intensity, an increase of sensitivity to the exposure frequency takes place. 2) Exposure to an intense tone does not apparently affect the sensitivity of the exposed animals to other frequencies. 3) The facts established by the experiment support a place-pitch or resonance theory of the perception of sound which regards the cochlea as the organ of pitch discrimination. 4) An explanation of the perception of intensity is offered by the linear spread of the disturbance set up in the basilar membrane by a stimulating sound, thus making the number of fibers stimulated a direct correlate of the intensity of the perceived tone.

Wever³⁴ presented repeated tones accompanied by electric shocks and found this adequate to induce a characteristic alteration in the animal’s respiration at the sounding of the tone. By this method (a form of conditioned-response audiometry) he investigated the upper limit of hearing of three cats, and found it between 10 and 20 kHz. Thus, he considered the cat’s capacity in the hearing of high tones similar to that of humans. Currently, it is well established that cats hear tones up to 40–45 kHz, which is at least an octave higher in frequency than the upper limit in humans.³⁵

1.2.3 Wever and Bray and after

The discussions about place vs. periodicity theories of hearing changed profoundly after the seminal publications by Wever and Bray³⁶,³⁷ on some experiments that were intended to test the limit of synchronous nerve impulses in the cat’s auditory nerve. Wever and Bray³⁶ found that sound stimuli applied to the ear of the animal produced neural activity, recorded from an electrode on the auditory nerve, that when amplified and reproduced by a telephone receiver was of great fidelity. Speech was easily understandable. Frequencies as high as 3,300 Hz were audible and did not appear distorted. Importantly, they used a reference electrode elsewhere on the body thereby allowing a large pick-up volume for neural activity. In a follow-up study, Wever and Bray³⁷ noticed that the discovery of impulses in the auditory nerve establishing a frequency as high as 4000 Hz represented a rate considerably above that previously found in any nerve. They pointed out that a high rate of impulses in the auditory nerve as a whole does not necessarily define the nature of refractory phase and hence the average rate of response in the individual fibers. They thought it possible for a high rate to be established by slowly acting fibers going off in volleys (Figure 1.2). This was the birth of Wever’s volley theory of hearing, fully developed in his 1949 book Theory of Hearing.²⁸

Figure 1.2 Sequential and superimposed responses of a single auditory nerve fiber showing phase-locking of action potentials in an auditory nerve fiber to a tone. One could conceive this repeated activity in one nerve fiber as representing the simultaneous activity of a group of auditory nerve fibers. Reprinted from,⁸⁷ with permission from Elsevier.

An early comment from Adrian³⁸ and later electrophysiological observations from Davis and collaborators³⁹,⁴⁰ strongly suggested, however, that Wever and Bray had measured a mixture of cochlear microphonics (later found to be the result of membrane potential changes in the hair cells that are synchronous with the frequencies of the sound) and nerve impulses, and that synchrony of the impulses was not preserved beyond 3000–4000 Hz. Note that Davis (1896–1992) studied with Adrian (1889–1977). Adrian criticized Wever and Bray’s interpretation of the effect³⁸:

The object of this note is to criticize their interpretation of the effect, but it is not intended to detract in any way from its interest. I have found no difficulty in reproducing most of their results, but I think it is almost certain that the electric changes are generated in the cochlea and are not due to nerve impulses.

Adrian replicated the effect in recordings from the auditory nerve surface, the medulla or the cerebellum and concluded that it could not be due to impulses in the nerve fibers under the electrode since it persisted unchanged after the nerve surface was covered with Novocain (a local anesthetic) or with ice (cooling prevents conduction of nerve impulses), thereby making it unable to generate action potentials. Adrian concluded that the effect must be some kind of microphonic action by which sound caused vibrations in the cochlea that produced potential changes between different points in the inner ear. With a needle electrode on the auditory nerve and a reference electrode on the body Saul and Davis⁴¹ confirmed the Wever and Bray experiment. However, when using concentric electrodes—i.e., the reference electrode shields the active electrode at short distance—they were able to distinguish at least three sources for the