Invited Review Evaluating the Perceptual and Pathophysiological
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JARO 12: 535–546 (2011) DOI: 10.1007/s10162-011-0271-6 D 2011 Association for Research in Otolaryngology JARO Invited Review Journal of the Association for Research in Otolaryngology Evaluating the Perceptual and Pathophysiological Consequences of Auditory Deprivation in Early Postnatal Life: A Comparison of Basic and Clinical Studies 1,2 1,2,3 JONATHON P. W HITTON AND DANIEL B. POLLEY 1Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, 243 Charles St, Boston, MA 02114, USA 2Harvard-MIT Division of Health Sciences and Technology, Speech and Hearing Bioscience and Technology Program, Cambridge, MA 02139, USA 3Department of Otology and Laryngology, Harvard Medical School, Boston, MA 02115, USA Received: 9 February 2011; Accepted: 2 May 2011; Online publication: 24 May 2011 ABSTRACT target the subset of children with a history of OM that is also accompanied by elevated hearing thresholds Decades of clinical and basic research in visual system consistently identify perceptual and physiological development have shown that degraded or imbal- deficits that can endure for years after peripheral anced visual inputs can induce a long-lasting visual hearing is audiometrically normal, in keeping with the impairment called amblyopia. In the auditory animal studies on CHL. These studies suggest that domain, it is well established that inducing a con- infants with OM severe enough to cause degraded ductive hearing loss (CHL) in young laboratory afferent signal transmission (e.g., CHL) are particu- animalsisassociatedwithapanoplyofcentral larly at risk to develop lasting central auditory impair- auditory system irregularities, ranging from cellular ments. We propose some practical guidelines to morphology to behavior. Human auditory depriva- identify at-risk infants and test for the positive tion, in the form of otitis media (OM), is tremen- expression of amblyaudia in older children. dously common in young children, yet the evidence linking a history of OM to long-lasting auditory Keywords: otitis media, conductive hearing loss, processing impairments has been equivocal for deca- auditory deprivation, development, plasticity, auditory des. Here, we review the apparent discrepancies in the cortex, binaural, dichotic, language, hearing, clinical and basic auditory literature and provide a listening, amblyopia, visual cortex, experience, meta-analysis to show that the evidence for human neural circuit amblyaudia, the auditory analog of amblyopia, is considerably more compelling than is generally believed. We argue that a major cause for this discrepancy is the fact that most clinical studies AN INTRODUCTION TO OTITIS MEDIA attempt to link central auditory deficits to a history AND AMBLYAUDIA of middle ear pathology, when the primary risk factor for brain-based developmental impairments such as Otitis media (OM) is a common childhood illness that amblyopia and amblyaudia is whether the afferent is characterized by purulence and/or the accumula- sensory signal is degraded during critical periods of tion of excessive mucin in the middle ear space. In brain development. Accordingly, clinical studies that some instances, the mechanical properties of the middle ear system can be altered by the presence of Correspondence to: Jonathon P. Whitton & Harvard-MIT Division of viscous fluid in the typically air-filled tympanum. In Health Sciences and Technology & Speech and Hearing Bioscience and Technology Program & Cambridge, MA 02139, USA. email: these cases, the auditory signal transmitted to the [email protected] developing central nervous system is degraded, 535 536 WHITTON AND POLLEY: Consequences of Auditory Deprivation in Early Postnatal Life prompting many clinicians and researchers to there is less consensus concerning the urgency of hypothesize that OM may represent a common form treating this disease. Common procedures to treat OM of developmental auditory deprivation. Dating back to include insertion of tympanostomy tubes, prescription the seminal studies of Hubel and Wiesel in the 1960s of oral antibiotics, and adenoid removal. As all inter- and 1970s, developmental sensory deprivation has ventions carry some level of risk, particularly with young repeatedly been shown to have specific, long-lasting, children, debate is focused on the benefits of alleviating and deleterious effects on brain and behavior. For OM versus waiting for it to resolve spontaneously. This is example, decades of basic and clinical research have particularly true in the case of OME, where the presence shown that improperly aligned visual signals trans- of middle ear effusion is not necessarily accompanied by mitted from each eye to the brain during critical infection or discomfort. At the crux of this controversy periods of central visual system development can lies the question of whether childhood OM is associated result in a neurological disorder known as amblyopia, with abnormal brainstem physiology and deficits in or “lazy eye”. However, establishing whether OM also spatial hearing as well as receptive language skills that induces persistent changes in brain physiology and persist for years after the middle ear pathology has perception in humans has proven more controversial. resolved, a cluster of neurological seqeulae we refer to In this meta-analysis, we compile findings from here as amblyaudia (amblyos—blunt; audia—hearing). decades of OM studies and argue that the key factor Should amblyaudia be acknowledged as a legitimate risk in the controversy can be explained by the fact that factor when OM is left untreated, it could shift the cost- most clinical studies only account for the presence of benefit analysis towards rapid intervention. On the OM and do not take the additional critical step of other hand, should the link to auditory processing determining whether the OM also imposes an appre- disorders be convincingly disproven, the decision to ciable conductive hearing loss (CHL). The minority intervene versus “watchful waiting” could be solely of clinical studies that have positively identified the based upon the peripheral symptoms. Although over subset of children with histories of OM and CHL offer 40 years have passed since Holm and Kunze (1969)first a significantly clearer and more sobering view of the reported deficiencies in multiple speech, language and connection between this common childhood hearing auditory tasks in a small sample of children with a history disorder and its enduring pathophysiological and of OM, a definitive answer regarding the connection perceptual sequelae. between OM and amblyaudia has yet to be firmly The strong interest in the prevention, treatment, established. To understand why the perceptual and and neurobiological sequelae of OM is in part pathophysiological sequelae of OM have proven so attributable to its high prevalence in children. In fact, controversial, it is principally important to understand an estimated 80% of children will experience one or the theoretical relationship between OM, hearing loss, more bouts of OM before they reach 3 years of age, and the maturation of auditory processing. making it the most common cause for physician visits Although OM is physically restricted to the middle and medication prescriptions among children in the ear space, it can interfere with the transmission of USA (Freid et al. 1998; Pennie 1998). Children can acoustic signals to the inner ear and, by extension, the experience OM in one or both ears, although bilateral entire auditory system. The middle ear pathology and OM is slightly more common (Engel et al. 1999). accumulation of excess, viscous mucin that typically Unilateral and bilateral bouts of otitis media with accompany OM can disrupt the acoustico-mechanical effusion (OME) persist for an average of 1 or properties of the middle ear system, producing a CHL 2 months, respectively (Hogan et al. 1997). A subset (Gravel and Wallace 2000; Ravicz et al. 2004). The of children (30–40%) experience recurrent OME, CHL that accompanies OM fluctuates between 0 and characterized by OME episodes of typical lengths 40 dB HL, is relatively uniform across frequencies and separated by unusually brief (10 weeks by contrast to is considered to be reversible in that hearing sensi- the typical 31 weeks) effusion-free periods (1997). tivity returns to normal following resolution of OM Because OME can occur without the painful symp- (Kokko 1974; Gravel et al. 2006). In addition to toms that accompany infection, it may often go attenuating the overall amplitude of the acoustic unnoticed by parents or caregivers without periodic signal, viscous fluid in the middle ear space can also otolaryngological and audiological assessments. delay transmission of the transduced waveform (Hartley Whether the diagnosis is acute OM, OME, or recur- and Moore 2003). Differences in the timing (interaural rent OME, its prevalence drops precipitously after time difference) and amplitudes (interaural level differ- 2 years of age and is rarely associated with signs of ence) of acoustic signals arriving at the two ears play an significant, lasting middle ear pathology (Gravel and essential role in spatial hearing, particularly in the Wallace 2000). horizontal plane. To illustrate the effects of OM- While the methods for diagnosing and treating OM mediated conductive hearing loss on spatial hearing, are generally agreed upon by health care practitioners, we can make approximations of azimuthal shifts relative WHITTON AND POLLEY: Consequences of Auditory Deprivation in Early Postnatal Life 537 to midline