Abstract and Keywords
This article introduces the fascinating complexity of the auditory brain: the neural centres and their connections that enable us to perceive and interpret sounds that have been transduced into neural activity by the cochlea. It reviews how different categories of stimuli are encoded and examines sounds that have the greatest biological significance. The reasons for changes in hearing throughout life are explored and this helps to predict that development might play an important role in the auditory brain because the sensory cues that an animal receives will change as the head grows. Sounds are more than just stimuli that are perceived, they have a considerable capacity to influence our emotional and cognitive states. Some aspects of these processes are analysed. Finally, this article considers disorders of the auditory brain and demonstrates that while most hearing loss has its origin in pathological changes in the cochlea, subtle deficits in auditory processing arise from lesions in specific regions of the auditory pathway.
The purpose of this volume is to introduce the reader to the fascinating complexity of what we have chosen to call the auditory brain: those neural centres and their connections that enable us to perceive and interpret sounds that have been transduced into neural activity by the cochlea.
Hearing, with its obvious link to language, is arguably the most important of all the senses in separating humans from other animals. The perception of sound underlies the enormous richness and complexity of our vocal communication, which, together with music, has been a primary driver of human intellectual and cultural development. However, long before we became creatures of the theatre or concert hall, hearing played an important part in our survival and evolution. Hearing alerted our ancestors to approaching predators, and signalled the presence of prey before it came in sight. Hearing not only allows us to detect the presence of such threats or opportunities, it also enables us to locate them; running in the direction of safety rather than into the jaws of the predator is an essential rule in winning the survival game! These vital advantages to humans and other animals that hearing provides makes stern demands on the system that is responsible for detecting and analysing the pressure waves that constitute sounds.
Vision, with a few exceptions, provides a limited view of an animal’s surroundings, and this is particularly true of primates, carnivores, and other species that have sacrificed visual field for depth perception. Foveal vision enables the animal to select the object to view. Hearing, on the other hand, always samples the whole sound field; even by turning the head, or in some animals rotating the ears, towards a sound source it is not possible to exclude sounds originating from other sources and directions. Thus separating and distinguishing sound sources are essential processes for hearing, and particular challenges for the auditory brain.
Another important difference between hearing and other senses (e.g. vision and somatosensation) is in the spatial representation of objects. In vision, objects at different points in space stimulate topographically equivalent positions on the receptor array in the retina. In contrast, the spatial position of a sound source is not mapped onto the hair cell receptors arrayed along the basilar membrane in the inner ear. The displacement of the basilar membrane reflects the frequency and level of the components of a sound, so sound source location, for the most part, must be computed in the brain utilizing cues that are extracted from the spectral, temporal, and level differences at the ears that arise from sounds occupying different positions in space. Perhaps for this reason alone the organization of the auditory system with its many subthalamic nuclei linked by a bewildering pattern of connections is more complex than the equivalent pathways for other senses.
Sounds are waveforms defined by pressure fluctuations in the medium through which they propagate, and they are thus inherently time dependent. They are in constant flux, and auditory objects cannot in their entirety be frozen into a brief glimpse. This fundamental physical property of sounds has required the auditory brain to evolve the capacity to encode time-dependent information with an exquisite precision that exceeds that of any other sensory system. Viewed from a (p. 2) particular instant in time, all information-bearing elements of sounds, like syllables or words, have a history and a future, and virtually all sounds that have any biological significance are characterized by time-dependent changes in their parameters.
For all these reasons, the auditory brain can be rather intimidating for the new student. This is exacerbated by the fact that central auditory processing is usually given only superficial coverage by most neuroscience textbooks, and there are few resources between that level and the primary sources to help a reader who seeks a more detailed understanding of the field. Another potential difficulty for the newcomer is the diverse range of techniques that are harnessed to study the brain. These range from methods that address the structural and functional properties of single cells, like immunocytochemistry and single unit recording, to functional magnetic resonance imaging (fMRI), magnetoencephalography (MEG) and behaviour that provide a window on the function of the brain in its entirety. One of the challenges for neuroscience is to discover how these multiple levels of brain organization are interrelated and lead to perception.
Our aim here has been to bring together, in a single volume, an account of what is known about the brain mechanisms that underlie different facets of hearing; their anatomy and physiology, what changes occur during development and ageing, and the consequences when they malfunction. We have commissioned succinct, up-to-date accounts of the current state of knowledge, written by experts in their field. We hope these will not only serve as an introduction for those who are exploring auditory processing for the first time, but also provide a valuable resource for experienced auditory scientists who want to know more about a field outside their speciality. The book is intended to give an overview of the field, to identify the main concepts and controversies, and provide sufficient orientation to enable the reader to plunge with confidence into the primary literature.
Research monographs often tackle the auditory pathway on a hierarchical centre-by-centre basis, beginning at the auditory nerve and working chapter by chapter towards the cortex. This approach often reflects each author’s focus of endeavour within the auditory pathway, and while useful to others studying the same brain area, it is less useful for the reader who wants to grasp the bigger picture. In contrast, each chapter in this volume explores its subject over the whole auditory pathway in an attempt to provide a more integrated account.
The organizing principle of the book is its arrangement into several themes that we believe define the field: how sounds are encoded for their identification and location; changes that occur in the auditory pathway throughout life; how sounds influence emotions, learning, and memory; and disorders of the auditory brain and its potential as a target for auditory prostheses.
Of course it is not possible to explore these functionally orientated themes without some scene setting that describes the anatomical substrate that underpins them. This is provided by Section 1 which outlines the anatomy of the auditory pathway and its synaptic organization, providing the contextual material on which the remainder of the book depends. Thus, Malmierca and Hackett (Chapter 2) describe the structural and functional organization of the ascending auditory pathway. They explain the location and cellular architecture of the auditory centres in the brainstem, thalamus, and cortex, together with the interconnecting pathways that carry the flow of information from the output of the cochlea to the cortex.
While this ascending, bottom-up pathway is clearly essential for sensation, it is also intuitively obvious, and increasingly apparent from experimental studies, that auditory perception relies extensively on past experience, attention, and emotional state analysed at higher levels of the pathway. The extensive, but often overlooked, network of descending, top-down connections whereby activity generated by these aspects of auditory processing can intercept and modify the upward flow of information is described by Schofield (Chapter 3).
(p. 3) In the final chapter in this section, Altschuler and Shore (Chapter 4) outline the roles of the many neurotransmitters and synaptic mechanisms that subserve the neuronal interactions in the auditory brain.
With this background in place, Section 2 addresses the theme of how sounds are encoded for their identification. Young (Chapter 5) tackles how spectrum and level, the most elemental properties of all sounds, are encoded. A significant part of this chapter discusses responses to pure tones, noise bursts, and other relatively simple stimuli. Such sounds have been invaluable probes for studying the auditory system, because the processing of sound begins with its analysis by frequency in the cochlea (see The Ear, Volume 1 of this Handbook). However, as is also apparent from Young’s chapter, the auditory system is remarkably nonlinear, so that responses to simple sounds often fail to predict responses to more complex sounds.
The remaining chapters in this section develop this theme of complexity. In Chapter 6, Malone and Schreiner describe how sounds whose amplitudes fluctuate with time are encoded at different levels of the auditory pathway. This chapter emphasizes that temporal information in sounds resides not just in the rapid pressure fluctuations that determine the spectral content, or fine structure, of the waveform, but also in the slower variations of amplitude that shape the waveform’s envelope.
Pitch is a quality that is so readily ascribed to many sounds, both simple and complex, that one might expect that pinpointing its manner of representation in the brain would be easy. Perhaps because so many facets of a stimulus can contribute to the pitch percept, understanding where and how it is encoded has proved elusive. Wang and Bendor (Chapter 7) reveal that neuronal recording and imaging techniques are now beginning to impact on this problem and provide evidence for brain areas specific for the analysis and representation of pitch.
The review of how different categories of stimuli are encoded is completed with two chapters that examine sounds that have the greatest biological significance; the sounds that animals generate themselves. In Chapter 8, Klug and Grothe focus on bats. These are particularly interesting species to study because they produce sounds not just for communication, but also for echolocating their prey. The auditory systems of these animals are beautifully adapted to these tasks, and thus provide a fascinating insight into how the auditory brain can become highly specialized, as well as revealing processing mechanisms of more general application.
Understanding how speech sounds are encoded and processed is of particular interest in understanding the human auditory system, and this is explored by Scott and Sinex (Chapter 9). Because it is unique to humans there are obvious limitations on the techniques we can apply to study the different brain centres involved. The advent of brain imaging in conscious humans has been a huge step forward for studying speech processing at the cortical level, but the technical limitations of such brain imaging techniques limit their usefulness for studying lower centres or for providing detailed neurophysiological mechanisms. Information about the responses of neurons to speech sounds currently is almost entirely limited to measurements made in animals and makes the assumption that the fundamental coding strategies in the mammalian auditory system are well conserved.
Sounds generated by people and animals are often characterized by the presence of many spectral components. In the real world, such sounds rarely occur in isolation, but in a cacophony of different, but similar sounds, as at the eponymous cocktail party. The challenge for the auditory brain is thus not just the recognition of isolated sounds, but also of segregation: components from a single source must be grouped together and segregated from those belonging to other sources. Given the overlap that often exists between frequency components originating from different sources, our capacity to form these auditory streams is remarkable, and far beyond the capability (p. 4) of any machine. Fishman and Steinschneider (Chapter 10) discuss how the brain might extract the cues upon which this process depends. It seems likely that we use top-down as well as bottom-up processing for this task. As discussed earlier, we know much less about the role of these descending influences in auditory processing, but the emerging story of this important aspect of the auditory brain is explored by He and Yu (Chapter 11).
Section 3 considers the second aspect of sound encoding, how sounds are located. Key to this process is that the ears are separated by the solid mass of the head and so sample the sound field differently. This arrangement leads to disparities in the timing and level of the sound waves between the ears, and Yin and Kuwada (Chapter 12) describe the neural circuits that can extract these cues to enable us to localize sounds in the horizontal plane. However, as May describes in Chapter 13, localizing sounds in the vertical plane relies on monaural mechanisms derived from cues generated by the interaction of the sound waves with the outer ear and the head. In Chapter 14, the final chapter in this section, Litovsky and McAlpine discuss how binaural mechanisms involved in locating sounds in space also make an important contribution to isolating single sound sources and segregating them from others.
Hearing, like most aspects of brain function, changes throughout life and these changes are examined in Section 4. It is easy to predict that development might play an important role in the auditory brain because the sensory cues that an animal receives will change as its head grows. In Chapter 15, Hartley and King discuss how the auditory brain matures during development and the impact that sensory experience during early life has on this process. Such plasticity in the auditory pathway was once believed only to occur during early development, but it is now recognized that plasticity also occurs in the adult animal. Irvine (Chapter 16) discusses how changing the input to the auditory brain, often as a consequence of an insult to the cochlea, can lead to a reorganization of neuronal connections and function. Much of the decline in hearing experienced with age is attributable to loss of function at the receptor level in the cochlea, but, as Frisina (Chapter 17) explains, processing in the auditory brain also declines during ageing because of changes in its intrinsic organization, as well as those induced by a reduced input.
Sounds are not just stimuli that we perceive; as anyone who has been reduced to tears by a piece of music can attest, they have a considerable capacity to influence our emotional and cognitive states. Some aspects of these processes are explored in Section 5. Weinberger (Chapter 18) discusses how the auditory cortex must be viewed as much more than just a sound analyser. Evidence shows that it is also a substrate of learning and memory, and thus directly influences the way sounds modify behaviour and cognitive state. Armony and LeDoux (Chapter 19) describe how the limbic system must be seen as an extension of the auditory brain, and they tease out the mechanisms whereby sounds contribute to our emotions.
The final section considers disorders of the auditory brain. While most hearing loss has its origin in pathological changes in the cochlea, subtle deficits in auditory processing arise from lesions in specific regions of the auditory pathway, or as a consequence of developmental or acquired disorders. In their survey of these conditions in Chapter 20, Griffiths et al. demonstrate that such cases can provide powerful insights into functional mechanisms of the auditory brain. The perception of phantom sounds known as tinnitus, an affliction bringing misery to many, is often associated with cochlear hearing loss. While sensorineural hearing loss is often a precipitating condition for tinnitus, recent research suggests that the origin of such phantom percepts lies in changes to the auditory brain, particularly the midbrain and cortex. How this condition manifests itself and the mechanisms that give rise to it are discussed by Eggermont (Chapter 21). In the past 25 years the astonishing success of cochlear implants has revolutionized the treatment of profound sensorineural deafness originating in the cochlea. In the final chapter (22) Shannon reports how this prosthetic technology can be taken a stage further by implanting electrodes directly into (p. 5) the brainstem or midbrain to provide benefit to those whose hearing loss results from bilateral loss of the auditory nerves.
While our intention is to represent as many different facets of the auditory brain as possible in one place, there are inevitably some gaps. For example, one area we have not been able to cover is the fascinating story that is emerging on multimodal interactions between the auditory brain and the other senses: perhaps these omissions can be included in a future edition.
We are immensely grateful to the authors who have contributed so much of their expertise and time to produce this volume. To produce a critical summary of a huge body of research within the confines of a short chapter is a difficult task, and we appreciate the generous spirit with which they accepted our editing to make them shorter still! We also wish to thank Martin Baum, our Editor at OUP, and his colleagues, for their help with the book’s production. We hope the result is a wide ranging and accessible survey that also provides the researcher, hearing professional, or student with sufficient depth to gain a true insight into the organization and function of the auditory brain. (p. 6)