Central Auditory System and Central Auditory Processing Disorders: Some Conceptual Issues

Central Auditory System and Central Auditory Processing Disorders: Some Conceptual Issues Dennis P. Phillips, Ph.D.1 ABSTRACT The central auditory system has both parallel and hierarchical afferent architectures. In the frequency domain, it is tonotopically constrained, and in the spatial domain, it is dominated by a representation of the contralateral acoustic hemifield. The functions supported by the afferent pathways can be somewhat overlapping, and the connectivity among the pathways is to some degree plastic. Partial deafferentation (in the form of high-frequency hearing loss) and behavioral experience are capable of causing alterations in tonotopic maps in the more rostral auditory system, even in adult animals. Central auditory processing is often frequency- specific. The temporal processes needed for normal auditory function are diverse, which is to be expected given the heterogeneous ways in which auditory events are disposed in time and encoded neurally. Central auditory pathologies need not respect structural or functional boundaries in the brain, and so should be expected to have idiosyncratic presentations. Man- agement strategies based on auditory training may exploit basic neuroplas- ticity, but more evidence is needed to substantiate any hypothesis of their differential efficacy in remediation of central auditory processing disorders or language and reading problems. KEYWORDS: Auditory neuroscience, neural representation, neural plasticity, temporal processing, perceptual architecture, auditory training Learning Outcomes: Upon completion of this article, the reader will (1) understand the basic design principles of the central auditory pathway, factors that can trigger plastic responses of the central auditory system, and the forms that those responses take; (2) comprehend the diverse range of functions embraced by the term central auditory processing, and the many levels at which specifically temporal processes contribute to hearing; and (3) appreciate some of the issues surrounding auditory training paradigms and their effectiveness. Management of Auditory Processing Disorders; Editor in Chief, Catherine V. Palmer, Ph.D.; Guest Editor, Gail D. Chermak, Ph.D. Seminars in Hearing, volume 23, number 4, 2002. Address for correspondence and reprint requests: Dennis P. Phillips, Ph.D., Professor, Hearing Research Laboratory, Department of Psychology, Dalhousie University, Halifax, NS, Canada B3H 4J1. E-mail: [email protected]. 1Hearing Research Laboratory, Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada. Copyright © 2002 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662. 00734-0451,p;2002,23,04,251,262,ftx,en;sih00219x. 251 252 SEMINARS IN HEARING/VOLUME 23, NUMBER 4 2002 An important key in coming to an ana- That information is then disseminated within lytic understanding of central auditory pro- three divisions of the cochlear nuclear com- cessing (CAP) and its disorders (CAPDs) is plex, and from there to a host of caudal audi- the complexity and dynamism of the central tory brainstem nuclei. Almost all of those pro- auditory nervous system (CANS) itself. The jections are strictly topographic, that is, they brain, of which the CANS is a relatively small preserve the general tonotopy (i.e., the spatial but highly integrated part, is even more com- arrangement of neurons according to the fre- plicated and dynamic. This architectural com- quency to which they are most sensitive) devel- plexity is what supports the diversity of central oped in the cochlea, and connections within auditory function and the brain’s capacity for more central nuclei are usually sufficiently local adaptation and learning. Consider the fol- to preserve (or enhance) the fine frequency lowing: the brain must support the detection, tuning of individual neurons. discrimination and localization of sound, the The divergent projection of the cochlear segregation of auditory figure from ground, per- nerve on the cochlear nucleus begins a pattern ceptual learning within new or familiar audi- of parallel processing, in the sense that afferent tory dimensions, recognition and identification information from the same cochlear sources is of the source, introspection about the perceived received and processed, largely independently, sound, and so on. by three nuclei at the same time. Those nuclei The detail of our neurophysiologic de- participate in separable and identifiable neural scriptions of CANS function and behavioral circuits. Some of them are involved in binaural descriptions of CAP is growing, as is our com- spatial hearing. Thus, some nuclei of the su- prehension of the links between those two lev- perior olivary complex receive tonotopically els of description. With these advances are constrained inputs from both ventral cochlear coming new insights into CAPDs in terms of nuclei and, through those routes, can serve as both their genesis and their phenomenology coincidence detectors for the timing and am- and, in turn, there is an emergence of new ways plitudes of stimuli at the two ears. Those inter- of thinking about management and remedia- aural parameters in turn are cues to sound tion. Because much of this information is new, source location in the horizontal plane. In this and because it barely scrapes the surface of the way, we see the development of hierarchical system’s structural and functional architecture, processing, because the convergence of input re- much of our understanding is still at a concep- sults in a serial growth in response complex- tual level. The purpose of this article is to ity—from a code for the timing and amplitude sketch some of these advances, to illustrate their of events at a given ear, to a cross-correlation of strengths and importance, and to make cau- those encoded events at the two ears. tionary remarks about some of them. What fol- The cells of the olivary nuclei do not just lows is, of necessity, a somewhat personal view inherit the properties of their inputs, but exe- that is not intended to cover all aspects of these cute operations on those inputs so that a new issues; it does assume a basic knowledge of the representation emerges. In this instance, the rep- CANS and CAP. resentation is of the interaural cues for source location, and because this is done within tonotopically constrained architecture, it follows THE CENTRAL AUDITORY that the processing is done on a frequency-by- NERVOUS SYSTEM frequency basis. There is an important behavioral outcome of this. As it happens, the magni- The afferent sensory input to the CANS is the tude of the interaural disparities in time and array of cochlear nerve cell axons from each of intensity vary not only with the eccentricity of the two ears. The cochlear transduction pro- the sound source, but also with frequency. Sound cess confers on each afferent fiber narrow fre- sources that are wideband in spectrum thus pro- quency tuning, and it is the role of each fiber to vide a rich supply of information about source encode the presence, amplitude and timing of location and, because the interaural disparity stimulus energy within its frequency passband.1,2 information is encoded tonotopically, the fre- CAS AND CAPD: CONCEPTUAL ISSUES/PHILLIPS 253 quency-specificity of the information is pre- patchy mosaic of smaller territories dedicated served in the brain. This provides a rich neural to other facets of stimulus representation (lo- representation from which to derive a percep- cation, amplitude, bandwidth, periodicity, and tual judgement, and it is for these reasons that so on). Second, many of the circuits in the af- behavioral sound localization acuity is far more ferent pathway have overlapping functions. acute for wideband sources than for tonal ones Thus, binaural convergence that initially occurs that provide only a single time and/or intensity in the superior olivary nuclei also may occur de disparity at the ears. novo in the auditory midbrain (and as far ros- The outputs of the olivary nuclei and the tral as the cortex5). These patterns of connec- projections of some cell groups within the tivity make it difficult to assign a unique locus cochlear nuclei are sent to the nuclei of the lat- to any particular central auditory function. It is eral lemniscus and/or to the inferior colliculus probably because of the multiple layers of bin- (auditory midbrain). Some of these projections aural interaction that lesion of the olivary nu- also are parallel in organization. For example, clei can leave the patterns of binaural input to the lateral superior olive projects contralater- cortical neurons nearly normal.6 Whether such ally upon both the dorsal nucleus of the lateral inputs can support normal neurophysiologic lemniscus and the inferior colliculus (with the coding of interaural disparity cues in the cortex former then projecting on to the latter). There currently is unknown. is also a hierarchical arrangement in this level of the projections, because some individual neurons of the inferior colliculus receive, for CENTRAL REPRESENTATIONS, example, input from both the dorsal cochlear PLASTICITY, AND BEHAVIORAL nucleus and the lateral superior olive, and thus PERFORMANCE inherit the properties of both.3 The inferior colliculus ultimately receives input from the There is some degree of plasticity in the pat- cochlear nuclei, olivary nuclei, and nuclei of terns of auditory afferent connectivity. Perhaps the lateral lemniscus. These inputs are often the most dramatic expressions of this have come bilateral, but the excitatory or inhibitory nature from studies in animals with neonatal cochlear of the connectivity is of a kind that preserves ablations in whom there can be marked re- and/or refines the sensitivity to interaural cues arrangement of connections from the surviving for sound location.2 The inferior colliculus pro- ear.7 The striking complexity of the brainstem jects on the thalamic medial geniculate body, pathways offers numerous opportunities for local which then supplies the afferent input to the shuffling of connections following neonatal auditory cortex. There is also a well-developed ablations.

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