In the auditory cortex, do neighbouring neurons receive similar input frow lower levels of processing? In the auditory cortex, neighbouring neurons tend to like sounds that are similar in frequency. We ask whether this is because neighbouring neurons receive similar input from lower levels of the brain (specifically the thalamus). If we zoom out and take a global view, we see that there is a general tendency for neighbouring neurons to receive similar inputs (i.e. thalamic inputs to neighbouring neurons tend to like similar frequencies). However, if we use high-resolution imaging techniques to zoom in on a particular bit of cortex, we find that the inputs to the cortex are relatively diverse (i.e. we see thalamic inputs from neurons that like very different frequencies). In other words, the thalamic inputs to a particular bit of auditory cortex look quite similar from far away, but look more different from close-up.

Vasquez-Lopez SA, Weissenberger Y, Lohse M, Keating P, King AJ, Dahmen JC (2017) Thalamic input to auditory cortex is locally heterogenous but globally tonotopic. Elife e25141 doi: 10.7554/eLife.25141

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Can ferrets wear earphones? Earphones make it possible to precisely control the sound heard by each ear. This allows us to simulate different forms of hearing loss and create virtual auditory environments. It also enables us to produce unnatural sounds that can create auditory illusions. All of these features make earphones an invaluable experimental tool for studying how the brain hears. In this paper, we created earphones that can be worn by ferrets. This is important because ferrets are one of the most important species for understanding the neuroscience of auditory learning and development.

Nodal FR, Keating P, King AJ (2010) Chronic detachable headphones for acoustic stimulation in freely moving animals. J Neurosci Methods 189:44-50.

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Do humans and neurons adapt to recent sound statistics? When people spend time listening to sounds that come from a very narrow range of locations (statisticians would call this a low-variance distribution), they become very sensitive to even small changes in sound location. On the other hand, if people spend time listening to sounds that come from a very wide range of locations (a high-variance distribution), they become less sensitive to small changes in sound location. An individual’s perception of sound location is also affected by the average (or mean) location of sounds heard immediately before. For example, if you hear lots of sounds on the left-hand side of space, a sound subsequently presented straight in front of you will sound like it is coming from the right. This paper was the first to show that these phenomena can be seen in human behaviour. But we also showed that similar phenomena are seen in the responses of neurons in the mid-brain (specifically the inferior colliculus). In conjunction with many other studies, this shows that our perceptions are influenced by previous experience.

Dahmen JC, Keating P, Nodal FR, Schulz AL, King AJ (2010) Adaptation to stimulus statistics in the perception and neural representation of auditory space. Neuron 66:937-948.

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How is sound localization affected by previous experience? Sound localization is an excellent model system for understanding the neural basis of auditory learning and adaptation. In particular, sounds heard previously affect auditory perception at multiple different timescales. This review article summarizes recent advances in our understanding of this topic.

King AJ, Dahmen JC, Keating P, Leach ND, Nodal FR, Bajo VM (2011) Neural circuits underlying adaptation and learning in the perception of auditory space. Neurosci Biobehav Rev 35:2129-2139.

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Can ferrets use different sound localization cues? Sound localization relies upon a variety of different cues. For example, when a sound is located on one side of the head, it will be louder in one ear than the other (known as an Interaural Level Difference). It will also arrive earlier at one ear than the other (an Interaural Time Difference). Humans are sensitive to both of these cues, which can be demonstrated easily with earphones. Using earphones that can be worn by ferrets, this paper showed that ferrets are also sensitive to both of these cues, and are almost as sensitive to these cues as humans. This further confirms the ferret as an excellent species for understanding the neural basis of hearing in humans.

Keating P, Nodal FR, Gananandan K, Schulz AL, King AJ (2013b) Behavioral Sensitivity to Broadband Binaural Localization Cues in the Ferret. Journal of the Association for Research in Otolaryngology : JARO 14:561-572.

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What happens to sound localization if you experience hearing loss during development? Approximately 80% of children experience some form of hearing loss before the age of 2. This is commonly caused by ‘glue ear’, which often produces a hearing loss in one ear. Sound localization in the horizontal plane typically relies on differences between the sound heard by each ear (so-called binaural cues) and is therefore impaired by this type of hearing loss. This paper shows that the brain (primary auditory cortex) can adapt to a developmental hearing loss in one ear without compromising its ability to use normal hearing if it is restored later in life.

In particular, the brain adapts by learning to rely more on the sound heard by the ear with normal hearing. This is possible because the pinna produces subtle changes in the quality of a sound that vary with direction (known as spectral cues), and the brain can use this to locate sounds using a single ear. Surprisingly, though, if we restore normal hearing later in life, the brain rapidly reverts to relying more on the differences between the sound heard by each ear. This means that the brain can learn different strategies for sound localization and switch between them depending on the circumstances.

Action on Hearing Loss and the Wellcome Trust wrote excellent articles on this research intended for non-scientists [AHL article, WT article].

Keating P, Dahmen JC, King AJ (2013a) Context-specific reweighting of auditory spatial cues following altered experience during development. Current Biology 23:1291-1299.

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What are the developmental effects of a hearing loss in one ear? The developing brain has a remarkable capacity for rewiring and learning. This review paper outlines recent advances in our understanding of how the developing auditory brain is shaped by experience, considering the impact of asymmetric hearing loss on sound localization.

Keating P, King AJ (2013) Developmental plasticity of spatial hearing following asymmetric hearing loss: context-dependent cue integration and its clinical implications. Frontiers in Systems Neuroscience 7:123.

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Does experience affect which cues to sound location are used at different sound frequencies? Humans locate low-frequency sounds using differences in the timing of sound heard by each ear (a sound presented on one side of the head takes longer to reach the far ear). At high frequencies, humans rely more on differences in the intensity of sound heard by each ear (a sound is louder in the ear closest to it). This paper shows that ferrets are very similar to humans in this respect (which is known as the Duplex theory of sound localization). With extensive training, ferrets can also learn to locate low-frequency sounds using differences in the intensity of sound heard by each ear. Previous experience therefore affects which cues to sound location are used at particular frequencies.

Keating P, Nodal FR, King AJ (2014) Behavioral sensitivity to binaural spatial cues in ferrets: evidence for plasticity in the duplex theory of sound localization. European Journal of Neuroscience 39:197-206.

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Can the developing auditory system adapt to hearing loss using multiple adaptive strategies? A hearing loss in one ear changes some of the cues to sound location (the binaural cues that rely on differences between the sound heard by each ear) but leaves others intact (the cues that rely only on the sound heard by the ear with normal hearing). Previously, we showed that developing ferrets adapt to a hearing loss in one ear by learning to rely more on the cues to sound location that are unaffected by hearing loss. We now show that these ferrets can also localize sounds correctly using the cues that have been changed by hearing loss. This means that the developing brain (primary auditory cortex) can use multiple adaptive strategies to adapt to hearing loss. It also helps explain some of the apparent differences between experiments in birds and mammals. This suggests that many different species may use the same adaptive strategies. Finally, our results provide insight into the way in which sound location is represented by populations of neurons in the brain. Previous work had suggested that sound location is represented by the difference in neural activity between the two hemispheres. Although this may be true at the level of the brainstem, it does not appear to be true in the cortex.

Keating P, Dahmen JC, King AJ (2015) Complementary adaptive processes contribute to the developmental plasticity of spatial hearing. Nature Neuroscience 18:185-187.

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Click here for a commentary on this article written by Shihab Shamma.

How is sound localization affected by previous experience? This review paper outlines recent advances in our understanding of this topic and identifies some of the most promising directions for future research.

Keating P, King AJ (2015) Sound localization in a changing world. Current opinion in neurobiology 35:35-43.

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