Localizing a sound source involves the detection and integration of various spatial cues present in the sound waves at each ear. Previous studies indicate that the brain circuits underlying sound localization are calibrated by experience of the cues available to each individual. Plasticity in spatial hearing is most pronounced during development but can also be demonstrated during adulthood under certain circumstances. Investigations into whether adult humans can adjust to reduced input in one ear and learn a new correspondence between interaural differences cues and directions in space have produced conflicting results. Here we show that humans of both sexes can relearn to localize broadband sounds with a flat spectrum in the horizontal plane after altering the spatial cues available by plugging one ear. In subjects who received daily training, localization accuracy progressively shifted back toward their pre-plug performance after 1 week of earplugging, whereas no improvement was seen if all trials were performed on the same day. However, localization performance did not improve on a task that used stimuli in which the source spectrum was randomized from trial to trial, indicating that monaural spectral cues are needed for plasticity. We also characterized the effects of the earplug on sensitivity to interaural time and level differences and found no clear evidence for adaptation to these cues as the free-field localization performance improved. These findings suggest that the mature auditory system can accommodate abnormal inputs and maintain a stable spatial percept by reweighting different cues according to how informative they are.

Accurate auditory localization relies on neural computations based on spatial cues present in the sound waves at each ear. The values of these cues depend on the size, shape, and separation of the two ears and can therefore vary from one individual to another. As with other perceptual skills, the neural circuits involved in spatial hearing are shaped by experience during development and retain some capacity for plasticity in later life. However, the factors that enable and promote plasticity of auditory localization in the adult brain are unknown. Here we show that mature ferrets can rapidly relearn to localize sounds after having their spatial cues altered by reversibly occluding one ear, but only if they are trained to use these cues in a behaviorally relevant task, with greater and more rapid improvement occurring with more frequent training. We also found that auditory adaptation is possible in the absence of vision or error feedback. Finally, we show that this process involves a shift in sensitivity away from the abnormal auditory spatial cues to other cues that are less affected by the earplug. The mature auditory system is therefore capable of adapting to abnormal spatial information by reweighting different localization cues. These results suggest that training should facilitate acclimatization to hearing aids in the hearing impaired.

Nodal FR, Kacelnik O, Bajo VM, Bizley JK, Moore DR, King AJ. Lesions of the auditory cortex impair azimuthal sound localization and its recalibration in ferrets. J Neurophysiol 103: 1209 -1225, 2010. First published December 23, 2009 doi:10.1152/jn.00991.2009. The role of auditory cortex in sound localization and its recalibration by experience was explored by measuring the accuracy with which ferrets turned toward and approached the source of broadband sounds in the horizontal plane. In one group, large bilateral lesions were made of the middle ectosylvian gyrus, where the primary auditory cortical fields are located, and part of the anterior and/or posterior ectosylvian gyrus, which contain higher-level fields. In the second group, the lesions were intended to be confined to primary auditory cortex (A1). The ability of the animals to localize noise bursts of different duration and level was measured before and after the lesions were made. A1 lesions produced a modest disruption of approach-to-target responses to short-duration stimuli (Ͻ500 ms) on both sides of space, whereas head orienting accuracy was unaffected. More extensive lesions produced much greater auditory localization deficits, again primarily for shorter sounds. In these ferrets, the accuracy of both the approach-totarget behavior and the orienting responses was impaired, and they could do little more than correctly lateralize the stimuli. Although both groups of ferrets were still able to localize long-duration sounds accurately, they were, in contrast to ferrets with an intact auditory cortex, unable to relearn to localize these stimuli after altering the spatial cues available by reversibly plugging one ear. These results indicate that both primary and nonprimary cortical areas are necessary for normal sound localization, although only higher auditory areas seem to contribute to accurate head orienting behavior. They also show that the auditory cortex, and A1 in particular, plays an essential role in training-induced plasticity in adult ferrets, and that this is the case for both head orienting responses and approach-to-target behavior.

The location of a sound source is derived by the auditory system from spatial cues present in the signals at the two ears. These cues include interaural timing and level differences, as well as monaural spectral cues generated by the external ear. The values of these cues vary with individual differences in the shape and dimensions of the head and external ears. We have examined the neurophysiological consequences of these intersubject variations by recording the responses of neurons in ferret primary auditory cortex to virtual sound sources mimicking the animal’s own ears or those of other ferrets. For most neurons, the structure of the spatial response fields changed significantly when acoustic cues measured from another animal were presented. This is consistent with the finding that humans localize less accurately when listening to virtual sounds from other subjects. To examine the role of experience in shaping the ability to localize sound, we have studied the behavioural consequences of altering binaural cues by chronically plugging one ear. Ferrets raised and tested with one ear plugged learned to localize as accurately as control animals, which is consistent with previous findings that the representation of auditory space in the midbrain can accommodate abnormal sensory cues during development. Adaptive changes in behaviour were also observed in adults, particularly if they were provided with regular practice in the localization task. Together, these findings suggest that the neural circuits responsible for sound localization can be recalibrated throughout life.

Conductive hearing loss produced by middle ear disease (MED) is very prevalent in the first 5 years of childhood. Both MED in children and prolonged ear plugging in animals lead to a binaural hearing impairment that persists beyond the duration of the peripheral impairment. However, after cessation of the MED, or removal of the ear plug, binaural hearing gradually improves. We suggest here that this improvement is a passive form of auditory learning. We also show that active auditory learning, through repetition of discrimination tasks, can accelerate performance increments, both after hearing loss and in unimpaired individuals. A more detailed understanding of auditory learning holds out the prospect of improving rehabilitation strategies for the language- and hearing-impaired.