British Medical Bulletin

This Article Abstract FREE Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (7) Request Permissions Disclaimer Google Scholar Articles by Moore, D. R Search for Related Content PubMed PubMed Citation Articles by Moore, D. R Related Collections Otolaryngology Social Bookmarking          What's this?

British Medical Bulletin 63:171-181 (2002)
© 2002 The British Council

Auditory development and the role of experience

David R Moore

University Laboratory of Physiology, Oxford, UK

	Abstract

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
The human ear is functionally mature shortly after birth, but the central auditory system continues to develop for at least the first decade of life. Current interest focuses on the relation between the very late developing aspects of hearing and other aspects of cognition and behaviour. While active neural input to the brain is essential during the very early stages of development, auditory experience is now thought to be a powerful influence on central function throughout an individual's lifespan. Studies of sound localization and hearing with two ears have shown the capacity of the auditory system to adapt to altered environmental cues, even into adulthood. This environmental influence may either be harmful, as during conductive deafness, or beneficial, as evidenced by the positive outcomes of auditory training.

	Introduction

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
Hearing in humans begins around the 22nd week of gestation (see Moore and Jeffery¹). At this stage, behavioural responses to sounds are produced only by intense airborne stimulation, since the fetus is in a highly sound-attenuated environment, the outer and middle ears are fluid-filled², and the cochlea and central auditory pathway are structurally and functionally immature. Following birth, sensitivity to sound is rapidly acquired, and many simple aspects of hearing achieve maturity during the first year. However, some aspects, such as sound localization and temporal processing, that seem to require more extensive processing in the central auditory system, do not achieve mature performance for many years, even into adolescence.

Many factors contribute to the relatively slow development of hearing: the environment, poor sound conduction, and incomplete neural development. Of these, it is neural development that has received the most attention, that has seen the most significant advancement in understanding, over the last 10 years, and that will form the focus of this review. I will present a synthesis of recent findings and thinking on the role that experience plays in shaping auditory function. The two volumes of the Springer Handbook of Auditory Research dealing with development³ and plasticity⁴ of hearing are more general accounts. Here, I will define ‘experience’ broadly to include the effects of both sensorineural and conductive hearing loss, as well as exposure to ‘passive’ auditory environments and ‘active’ auditory training and learning. While early auditory experience is still considered especially critical for normal development, a major change of thought in the last 10 years has been the recognition of a life-time dependency on auditory input, and the ability of the mature system to respond to clinical or experimental manipulation of that input.

	Development of the auditory nervous system

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
The neural basis of hearing begins in the cochlear hair cells, where transduction channels in the tips of stereocilia pass K⁺ and other cations in response to mechanical displacement of the organ of Corti (see reviews by Richardson and by Ashmore, this volume). The electrical driving force behind the transduction current, the endocochlear potential of the scala media, begins to function only a short period before the onset of functional hearing⁵. At the same time, the cochlear partition is maturing structurally, in a basal-to-apical direction. Paradoxically, the earliest neural responses recorded from the central auditory system are evoked by low frequency sounds (e.g. Aitkin and Moore⁶). This appears to result from an immaturity of cochlear mechanics, such that the peak of the travelling wave along the cochlear partition produced by a given frequency occurs more basally than is the case in adults⁷. Other significant neural developments in the cochlea include changes in the size and shape of the hair cells, and the acquisition of mature synaptic function. These latter developments impair initial auditory function by limiting, respectively, the highest stimulus frequency at which auditory neurones can phase lock, and the maximum rate of firing of single auditory nerve fibres⁸. In short, there are known structural and functional restrictions on the ability of the cochlea to function at all before a certain age, and to function in an adult-like way for some further period. It is not completely clear how long these developmental processes take in humans, but peripheral auditory function appears to mature by the end of the first few post-natal months (Fig. 1A)^9,10.

View larger version (18K): [in this window] [in a new window]   Fig. 1 Development of human central auditory physiology. Auditory evoked potentials recorded from (A) the auditory nerve (wave N1 of the compound action potential) were, in terms of response latency (shown here, relative to adult values) and amplitude to tone stimuli, mature by the sixth postnatal month (0.5-year-old [y.o.]). The difference in latency between waves V and I of the auditory brainstem response (V–I) is a measure of conduction time from the cochlea to the midbrain. A substantial reduction in this conduction time occurred between a group tested at birth (0 y.o.) and a group tested at 6–24 months. Extrapolation of the V–I data yielded a final maturation age of 15–24 months, with responses to lower frequency tones developing more rapidly. In the auditory cortex (B), the N1 and P1 responses (see text) to click stimuli underwent substantial development into the second decade of life. Again, the measure is response latency, referenced to values for adult listeners. Adapted from Ponton et al9,11.

 
Developmental changes of function in the central auditory system, by contrast, appear to continue for several years. Neurones throughout the system show mature responses to single tones relatively soon after cochlear function begins¹² and, indeed, the capacity for neural function may precede that of cochlear function (see Romand¹³). However, hearing of some more complex sounds, such as temporally separated pairs^14,15, and performance on higher demand listening tasks (e.g. sound localization¹⁶) may remain immature well into the second decade of life (see Ponton et al¹¹). One important, and increasingly recognised, issue in the interpretation of behavioural studies of hearing is the extent to which performance reflects sensory and non-sensory factors. Cognitive influences (e.g. attention) may be developing in parallel with sensation and, without appropriate experimental control, give a misleading impression of immature function in the auditory system. On the other hand, a strict distinction between sensory and non-sensory influences on perception, even at relatively low levels of the brain, has recently been called into question by neuro-imaging studies of the human visual cortex¹⁷. Nevertheless, physiological studies in anaesthetised animals¹⁸ and in awake humans¹¹ of neural responses to dichotic (i.e. binaurally discordant) or rapidly presented sounds suggest that much of the immaturity of hearing seen after birth does have a sensory basis, in the conventional sense.

The protracted immaturity of the human central auditory system (Fig. 1B) could be caused by several known factors. Both morphological¹⁹ and physiological studies^9,11 indicate that development beyond the second to third year is a property of the higher, thalamocortical auditory system. While cortical cyto-architecture develops early, myelination of the thalamic fibres innervating the auditory cortex begins around one year of age and progresses until the fourth year. Expression of cortical neurofilament protein, forming the basis of the axonal cytoskeleton, continues to change through to the age of 5–10 years¹⁹. Conduction pathways are, therefore, immature for a protracted period of postnatal life and this will, of course, affect neural functions, such as auditory temporal processes. However, recent auditory evoked potential studies suggest that human thalamocortical function, as measured by the long-latency (40–200 ms) P₁ – N₁ – P₂ response sequence, continues to develop ‘well into adolescence’ according to Ponton et al¹¹. Although the later components of these compound responses are notoriously difficult to localize, the P₁ response is thought to originate predominantly from the lateral portion of Heschl's gyrus and, therefore, represents a relatively ‘low’ level of auditory processing. Nevertheless, the P₁ and N₁ responses do not reach maturity until 14–15 years of age. The very late development of these responses, which involve a decrease in both amplitude and latency, may be related to decreasing synaptic density and dendritic elaboration in the auditory cortex²⁰. However, insufficient anatomical data are available in the 5–15-year-old age range to form more definite conclusions.

	The nature of auditory experience

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
We generally think of auditory experience as the sounds we hear. But neuroscientists think in terms of neural activity generated in the cochlea and transmitted to the brain (Fig. 2). Environmental sound (e.g. speech) will modulate and increase auditory nerve activity, conductive hearing loss (e.g. otosclerosis, otitis media) will decrease and desynchronize nerve activity, and sensorineural loss will reduce and broaden, or abolish nerve activity from damaged parts of the cochlea. The brain is affected by these input fluctuations in two ways. The first is, of course, that it will pass the information to, and through, the various centres of the auditory system for processing, and on into the cortex for understanding, integration and action (see Palmer and Summerfield, this volume). The second is that it will change the way in which the brain processes future input. These latter changes may be either beneficial, as occurs during developmental shaping of speech processing circuits, or detrimental, as when lack of stimulation produced by (untreated) deafness leads to neurodegeneration. In the following sections, I discuss in more detail recent thinking about these two contrasting roles of auditory experience in shaping the function of the auditory brain.

View larger version (24K): [in this window] [in a new window]   Fig. 2 Auditory experience may be thought of as neural activity generated in the cochlea and transmitted to the brain. Removal of auditory (VIIIth) nerve activity early in life abolishes glutamate (Glu) neurotransmission and causes some auditory brain stem neurones to die and some to survive. In the chicken cochlear nucleus (CN), the cellular processes underlying this experience-dependent regulation have been worked out in some detail. In the synapse, de-activation of metabotropic glutamate receptors (mGluRs) signals an increase in intracellular calcium levels via the AMPAR type of glutamate receptors. Neurones destined to die undergo other rapid responses to the de-activation, including ribosomal disaggregation and a decrease in amino acid incorporation. If input is restored within 1–2 days, the neurones can return to normal. Neurones that do not die nevertheless undergo a number of responses including soma shrinkage and an increase, followed by a decrease, of oxidative metabolism and mitochondrial density. Recently, an increased phosphorylation of a transcription factor (CREB) has been demonstrated. This may lead to compensation for the activity deprivation and thence to neurone survival. Again, if input is restored, the neurones can return to normal. Adapted from Garden et al48 and Zirpel et al49.

 

	Bad auditory experience

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
The notion of ‘critical’ or ‘sensitive’ periods of development is well over 100 years old, but it is one that has undergone substantial recent revision. In hearing, there has been much progress in defining and characterizing a very early period during which clinical, surgical or chemical de-afferentation, resulting in total abolition of nerve activity, leads to wide-spread neurodegeneration in brain centres normally receiving direct input from the deaf ear (Fig. 2). In the cochlear nucleus of rodents, 50–70% of neurones have been found to die following cochlear removal before postnatal day (P) 10, where hearing begins at about P12^21,22. This apoptotic neurone death is but the end stage of a complex cascade of intracellular events that is triggered within minutes of activity withdrawal. However, just before the time at which hearing normally begins, the short-term dependence of auditory neurones on afferent activity abruptly stops. Thereafter, total deafening leads to shrinkage of neurones, probably due to membrane responses to axon retraction, but little or no death of target neurones, at least over a time course of months to years. One rationale for early cochlear implantation has been the need to provide trophic support for central auditory neurones in the absence of afferent activity. The early cessation of extreme sensitivity to de-afferentation suggests the importance of providing that support very early in development, and a reduced urgency for support thereafter.

Sensitive periods for some other aspects of auditory system plasticity have been more difficult to establish, especially where the change in auditory experience has consisted of a conductive hearing loss or a modification of the auditory environment. In addition, there has been a general realisation in neuroscience over the last decade that some aspects of the brain's susceptibility to experience-dependent plasticity are maintained throughout life. This will come as no surprise to those familiar with the well-known capacity in the elderly for recovery from stroke. However, there has been a great increase recently in the power of methods available for observing and measuring the plasticity. The new technology includes functional magnetic resonance imaging (fMRI) in humans (see Griffiths, this volume), and direct, optical imaging of the living brains of animals²³.

The plasticity of binaural and spatial hearing has been studied behaviourally, using psycho-acoustic methods, and physiologically²⁴. Although binaural hearing may be adversely affected by unilateral or asymmetric hearing loss, there is no clear evidence, in mammals, for an elevated susceptibility of the developing binaural system to abnormal experience. Clinically, both otosclerosis in adults and otitis media with effusion (OME) in children perturb binaural hearing. More surprisingly, poor auditory function at any age may persist beyond the time of the peripheral pathology^25,26. These effects have also been demonstrated in the laboratory. For example, prolonged ear plugging can lead to poor sound localization and binaural unmasking, a measure of the detection of sounds in noisy environments (Fig. 3)^24,27. When the plug is inserted, some adaptation (recovery of function) may occur but, following removal of the plug, performance may remain impaired. These results suggest that impoverished auditory experience produces a protracted difficulty in detecting sounds in noisy environments. This difficulty may contribute to the early language processing problems that have been reported²⁸ in some children with severe, recurrent OME.

View larger version (19K): [in this window] [in a new window]   Fig. 3 Unilateral or asymmetric conductive hearing loss, as seen in middle ear disease in children and otosclerosis in adults, can lead to poor binaural hearing. In the laboratory, these diseases are modelled using ear plugs in experimental animals to control for variability and to investigate mechanisms. Ferrets receiving several months of unilateral ear plugging had reduced binaural unmasking for several more months after the plug was removed (A; adapted from Moore et al27). Sound localization abilities (B; from King et al24) show adaptation to the plug during plugging (as shown in the figure) but, surprisingly, there is no lasting impairment after plug removal. The latter result suggests that, in this case, altered experience leads to the formation of a parallel neural representation (‘map’) of space, rather than to re-ordering of an existing map.

 

	Good auditory experience

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
The adaptive plasticity of the brain appears capable both of mediating recovery of auditory function after hearing loss and of improving function following auditory training. Children who have had recurrent OME, and who have persistent, impaired binaural hearing, gradually recover normal binaural function^29,30. Adult human listeners who have the normal cues for sound localization distorted gradually ‘adapt’ to the new cues and regain normally accurate localization^31,32. Most interestingly, ferrets that have had their auditory spatial localization disrupted by unilateral ear plugging gradually improve their localization if left in the home cage³³. If, however, they are given additional training in sound localization, the improvement occurs more rapidly.

Each of these cases provides compelling evidence for an experience-dependent improvement in spatial hearing following earlier maladjustment. That the improvement is at least partly mediated by auditory system neural plasticity is suggested by animal experiments showing that a neural ‘map’ of auditory space in the midbrain is shifted by manipulating the input from the ears in a way that is predictable from the localization behaviour. In the barn owl, for example, recent experiments³⁴ have shown frequency-specific changes in the tuning of midbrain neurones to the binaural cues underlying sound localization following several months of wearing an acoustic device that alters the time and level cues independently. Other experiments on the plasticity of spatial hearing mechanisms in mammals suggest that neurones in both the midbrain³⁵ and the auditory cortex³⁶ are influenced by prior auditory experience.

Enhanced auditory experience has recently been shown to be a useful therapeutic tool. For many years, it has been known that subjects in psycho-acoustic and other sensory tasks improve their performance with practice. When those practice effects have been applied to training listening skills in children with language impairments, dramatic results have been reported^37,38; (but see review by Bailey and Snowling, this volume). While the therapeutic effectiveness of this approach appears to be impressive, it is unclear whether the technique works through auditory perceptual learning or, more indirectly, through building up attention and other more general sensorimotor skills. Perceptual learning is thought to be highly specific to the trained stimulus, at least for some types of task³⁹. A recent study that trained adults in the time and level cues for sound localization⁴⁰ has shown that the long-term, intensive training that is often considered necessary to obtain robust improvements is specific both for the stimulus frequency used during training and the type of cue trained. These findings suggest that sensory training will only be practically effective if the trained stimuli closely resemble the skill that the training is designed for. In the case of language training, this seems to indicate the use of appropriate linguistic stimuli rather than simpler signals of the type usually used in auditory research.

Deprivation followed by enhancement of ‘auditory’ experience in profoundly deaf people fitted with cochlear implants is thought to lead to the same cycle, and mechanisms, of neurodegeneration and recovery found in other examples of adaptive plasticity⁴¹. Traditionally, the focus of interest in implantation has centred on the design of the speech processor and how that interfaces with remaining neural elements in the cochlea. It is now more widely recognised that both the problem (deafness) and the solution (implantation) are also dependent on the central auditory system. For example, recent studies have shown that activation of the auditory cortex in congenitally deaf cats is substantially enhanced by long-term electrical stimulation of the cochlea. Animals deafened and stimulated at later ages seem not to respond as well to implantation, but it is unclear to what extent that limitation is due to more peripheral effects of the deafening⁴².

Neuro-imaging techniques are beginning to capture the changes in brain activation in humans that accompany impaired or enhanced auditory experience. Unilateral, congenital deafness leads to changes in the symmetry of auditory cortex fMRI activation produced by stimulation of the functional ear⁴³. Experience of cochlear implantation in adults following post-lingual deafness modifies activation of the auditory and temporal cortices⁴⁴. Individuals with impaired auditory and/or linguistic function have correlated perturbations of sound processing in the auditory cortex^45,46. Audiovisual training, matching simple non-linguistic sound sequences to patterns of rectangles on a computer screen, has been found to improve both reading skills and an electrophysiological indicator of cortical function (the ‘mismatch negativity’) in dyslexic children⁴⁷. While these efforts to study the ‘mechanisms’ of auditory system plasticity are exciting, the results need to be interpreted with considerable caution. As noted above, it is not always clear just what aspect of the life experience of the affected individuals has led to the impaired, or enhanced, function. It is also uncertain how the changes in observed activation relate specifically to auditory function. From the viewpoint of auditory experience, it is also sometimes unclear what the direction of causation is when relating patterns of activation to hearing. Nevertheless, careful improvements in experimental design, and continually evolving technology, including data from two or three techniques (e.g. fMRI and auditory evoked potentials) for a single listener, hold the promise of significant advances in understanding the neural basis of auditory system plasticity over the coming few years.

	Acknowledgements

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 
I thank the Medical Research Council, the Wellcome Trust, Defeating Deafness, the John Ellerman Foundation, and the National Health Service for supporting our research. Doug Hartley, Sarah Hogan, Andy King, Carl Parsons, Jan Schnupp, Travis Tierney and Huib Versnel collaborated on work from our laboratory described in this paper.

	Footnotes

 
Correspondence to: Prof. David R Moore, University Laboratory of Physiology, Parks Road, Oxford OX1 3PT, UK

	References

Top Abstract Introduction Development of the auditory... The nature of auditory... Bad auditory experience Good auditory experience Acknowledgements References

 

1. Moore DR, Jeffery G. Development of auditory and visual systems in the fetus. In: Thorburn GD, Harding R. (eds) Textbook of Fetal Physiology. Oxford: Oxford University Press, 1994; 278–86
2. Sohmer H, Perez R, Sichel JY, Priner R, Freeman S. The pathway enabling external sounds to reach and excite the fetal inner ear. Audiol Neurootol 2001; 6: 109–16[Medline]
3. Rubel EW, Popper AN, Fay. RR (eds) Development of the Auditory System. Springer Handbook of Auditory Research, vol. 9, New York: Springer, 1998
4. Parks TN, Rubel EW, Popper AN, Fay RR. (eds) Plasticity of the Auditory System. Springer Handbook of Auditory Research, vol. 10. New York: Springer, 2002
5. Rübsamen R, Lippe WR. The development of cochlear function. In: Rubel EW, Popper AN, Fay RR. (eds) Development of the Auditory System. Springer Handbook of Auditory Research, vol. 9, New York: Springer, 1998; 193–270
6. Aitkin LM, Moore DR. Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. J Neurophysiol 1975; 38: 1208–16[Abstract/Free Full Text]
7. Mills DM, Rubel EW. Development of the base of the cochlea: place code shift in the gerbil. Hear Res 1998; 122: 82–96[ISI][Medline]
8. Kettner RE, Feng JZ, Brugge JF. Postnatal development of the phase-locked response to low frequency tones of auditory nerve fibers in the cat. J Neurosci 1985; 5: 275–83[Abstract]
9. Ponton CW, Eggermont JJ, Coupland SG, Winkelaar R. Frequency-specific maturation of the eighth nerve and brain-stem auditory pathway: evidence from derived auditory brain-stem responses (ABRs). J Acoust Soc Am 1992; 91: 1576–86[ISI][Medline]
10. Eggermont JJ, Brown DK, Ponton CW, Kimberley BP. Comparison of distortion product otoacoustic emission (DPOAE) and auditory brain stem response (ABR) traveling wave delay measurements suggests frequency-specific synapse maturation. Ear Hear 1996; 17: 386–94[ISI][Medline]
11. Ponton CW, Eggermont JJ, Kwong B, Don M. Maturation of human central auditory system activity: evidence from multi-channel evoked potentials. Clin Neurophysiol 2000; 111: 220–36[ISI][Medline]
12. Sanes DH, Walsh EJ. The development of central auditory processing. In: Rubel EW, Popper AN, Fay RR. (eds) Development of the Auditory System. Springer Handbook of Auditory Research, vol. 9, New York: Springer, 1998; 271–314
13. Romand R. Development of Auditory and Vestibular Systems. New York: Academic Press, 1983
14. Trehub SE, Schneider BA, Henderson JL. Gap detection in infants, children, and adults. J Acoust Soc Am 1995; 98: 2532–41[ISI][Medline]
15. Hartley DE, Wright BA, Hogan SC, Moore DR. Age-related improvements in auditory backward and simultaneous masking in 6- to 10-year-old children. J Speech Lang Hear Res 2000; 43: 1402–15[Abstract/Free Full Text]
16. Litovsky RY. Developmental changes in the precedence effect: estimates of minimum audible angle. J Acoust Soc Am 1997; 102: 1739–45[ISI][Medline]
17. Ress D, Backus BT, Heeger DJ. Activity in primary visual cortex predicts performance in a visual detection task. Nat Neurosci 2000; 3: 940–5[ISI][Medline]
18. Eggermont JJ. Differential maturation rates for response parameters in cat primary auditory cortex. Aud Neurosci 1996; 2: 309–27
19. Moore JK, Guan YL. Cytoarchitectural and axonal maturation in human auditory cortex. J Assoc Res Otolaryngol 2001; 2: 297–311[Medline]
20. Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 1997; 387: 167–78[ISI][Medline]
21. Tierney TS, Russell FA, Moore DR. Susceptibility of developing cochlear nucleus neurones to deafferentation-induced death abruptly ends just before the onset of hearing. J Comp Neurol 1997; 378: 295–306[ISI][Medline]
22. Mostafapour SP, Del Puerto NM, Rubel EW. bcl-2 Overexpression eliminates deprivation-induced cell death of brainstem auditory neurons. J Neurosci 2002; 22: 4670–4[Abstract/Free Full Text]
23. Versnel H, Mossop JE, Mrsic-Flögel T, Ahmed B, Moore DR. Optical imaging of intrinsic signals in ferret auditory cortex: responses to narrow-band sound stimuli. J Neurophysiol 2002; In press
24. King AJ, Parsons CH, Moore DR. Plasticity in the neural coding of auditory space in the mammalian brain. Proc Natl Acad Sci USA 2000; 97: 11821–8[Abstract/Free Full Text]
25. Hall JW, Grose JH. Short-term and long-term effects on the masking level difference following middle ear surgery. J Am Acad Audiol 1993; 4: 307–12[Medline]
26. Hogan SC, Moore DR. Impaired binaural hearing in children produced by a threshold level of middle ear disease. J Assoc Res Otolaryngol 2002; In press
27. Moore DR, Hine JE, Jiang ZD, Matsuda H, Parsons CH, King AJ. Conductive hearing loss produces a reversible binaural hearing impairment. J Neurosci 1999; 19: 8704–11[Abstract/Free Full Text]
28. Bluestone CD, Klein JO. Otitis Media in Infants and Children, 2nd edn. Philadelphia, PA: WB Saunders, 1995
29. Hall JW, Grose JH, Pillsbury HC. Long-term effects of chronic otitis media on binaural hearing in children. Arch Otolaryngol Head Neck Surg 1995; 121: 847–52[Abstract]
30. Hogan SC, Meyer SE, Moore DR. Binaural unmasking returns to normal in teenagers who had otitis media in infancy. Audiol Neurootol 1996; 1: 104–11[Medline]
31. Hofman PM, Van Riswick JG, Van Opstal AJ. Relearning sound localization with new ears. Nat Neurosci 1998; 1: 417–21[ISI][Medline]
32. Shinn-Cunningham BG, Durlach NI, Held RM. Adapting to supernormal auditory localization cues. I. Bias and resolution. J Acoust Soc Am 1998; 103: 3656–66[ISI][Medline]
33. King AJ, Kacelnik O, Mrsic-Flögel TD, Schnupp JW, Parsons CH, Moore DR. How plastic is spatial hearing? Audiol Neurootol 2001; 6: 182–6[Medline]
34. Knudsen EI, Zheng W, DeBello WM. Traces of learning in the auditory localization pathway. Proc Natl Acad Sci USA 2000; 97: 11815–20[Abstract/Free Full Text]
35. Schnupp JW, King AJ, Carlile S. Altered spectral localization cues disrupt the development of the auditory space map in the superior colliculus of the ferret. J Neurophysiol 1998; 79: 1053–69[Abstract/Free Full Text]
36. Mrsic-Flögel TD, King AJ, Jenison RL, Schnupp JW. Listening through different ears alters spatial response fields in ferret primary auditory cortex. J Neurophysiol 2001; 86: 1043–6[Abstract/Free Full Text]
37. Merzenich MM, Jenkins WM, Johnston P, Schreiner C, Miller SL, Tallal P. Temporal processing deficits in language-learning impaired children ameliorated by training. Science 1996; 271: 77–81[Abstract]
38. Tallal P, Miller SL, Bedi G et al. Language comprehension in language-learning impaired children improved with acoustically modified speech. Science 1996; 271: 81–4[Abstract]
39. Wright BA, Buonomano DV, Mahncke HW, Merzenich MM. Learning and generalization of auditory temporal-interval discrimination in humans. J Neurosci 1997; 17: 3956–63[Abstract/Free Full Text]
40. Wright BA, Fitzgerald MB. Different patterns of human discrimination learning for two interaural cues to sound-source location. Proc Natl Acad Sci USA 2001; 98: 12307–12[Abstract/Free Full Text]
41. Shepherd RK, Illing RB. Cochlear implants and brain plasticity. Audiol Neurootol 2001; 6: 299–396
42. Kral A, Hartmann R, Tillein J, Heid S, Klinke R. Delayed maturation and sensitive periods in the auditory cortex. Audiol Neurootol 2001; 6: 346–62[Medline]
43. Scheffler K, Bilecen D, Schmid N, Tschopp K, Seelig J. Auditory cortical responses in hearing subjects and unilateral deaf patients as detected by functional magnetic resonance imaging. Cereb Cortex 1998; 8: 156–63[Abstract/Free Full Text]
44. Giraud AL, Truy E, Frackowiak R. Imaging plasticity in cochlear implant patients. Audiol Neurootol 2001; 6: 381–93[Medline]
45. Temple E, Poldrack RA, Protopapas A et al. Disruption of the neural response to rapid acoustic stimuli in dyslexia: evidence from functional MRI. Proc Natl Acad Sci USA 2000; 97: 13907–12[Abstract/Free Full Text]
46. Ahissar E, Nagarajan S, Ahissar M, Protopapas A, Mahncke H, Merzenich MM. Speech comprehension is correlated with temporal response patterns recorded from auditory cortex. Proc Natl Acad Sci USA 2001; 98: 13367–72[Abstract/Free Full Text]
47. Kujala T, Karma K, Ceponiene R et al. Plastic neural changes and reading improvement caused by audiovisual training in reading-impaired children. Proc Natl Acad Sci USA 2001; 98: 10509–14[Abstract/Free Full Text]
48. Garden GA, Canady KS, Lurie DI, Bothwell M, Rubel EW. A biphasic change in ribosomal conformation during transneuronal degeneration is altered by inhibition of mitochondrial, but not cytoplasmic protein synthesis. J Neurosci 1994; 14: 1994–2008.[Abstract]
49. Zirpel L, Janowiak MA, Veltri CA, Parks TN. AMPA receptor-mediated, calcium-dependent CREB phosphorylation in a subpopulation of auditory neurons surviving activity deprivation. J Neurosci 2000; 20: 6267–75.[Abstract/Free Full Text]

CiteULike    Connotea    Del.icio.us    What's this?

This article has been cited by other articles:

				A. M. Patel, L. D. Cahill, J. Ret, V. Schmithorst, D. Choo, and S. Holland Functional Magnetic Resonance Imaging of Hearing-Impaired Children Under Sedation Before Cochlear Implantation Arch Otolaryngol Head Neck Surg, July 1, 2007; 133(7): 677 - 683. [Abstract] [Full Text] [PDF]

				R. Metherate Nicotinic Acetylcholine Receptors in Sensory Cortex Learn. Mem., January 1, 2004; 11(1): 50 - 59. [Abstract] [Full Text] [PDF]

				K. Emmorey, J. S. Allen, J. Bruss, N. Schenker, and H. Damasio A morphometric analysis of auditory brain regions in congenitally deaf adults PNAS, August 19, 2003; 100(17): 10049 - 10054. [Abstract] [Full Text] [PDF]

This Article Abstract FREE Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (7) Request Permissions Disclaimer Google Scholar Articles by Moore, D. R Search for Related Content PubMed PubMed Citation Articles by Moore, D. R Related Collections Otolaryngology Social Bookmarking          What's this?

Online ISSN 1471-8391 - Print ISSN 0007-1420

Copyright © 2008 Oxford University Press

Oxford Journals Oxford University Press

• Site Map
• Privacy Policy
• Frequently Asked Questions

Other Oxford University Press sites: Oxford University Press Oxford Journals Japan American National Biography Booksellers' Information Service Children's Fiction and Poetry Children's Reference Corporate & Special Sales Dictionaries Dictionary of National Biography Digital Reference English Language Teaching Higher Education Textbooks Humanities International Education Unit Law Medicine Music Online Products Oxford English Dictionary Reference Rights and Permissions Science School Books Social Sciences Very Short Introductions World's Classics