Elsevier

Hearing Research

Volume 271, Issues 1–2, January 2011, Pages 54-65
Hearing Research

Research paper
Evolutionary conservation and neuronal mechanisms of auditory perceptual restoration

https://doi.org/10.1016/j.heares.2010.05.011Get rights and content

Abstract

Auditory perceptual ‘restoration’ occurs when the auditory system restores an occluded or masked sound of interest. Behavioral work on auditory restoration in humans began over 50 years ago using it to model a noisy environmental scene with competing sounds. It has become clear that not only humans experience auditory restoration: restoration has been broadly conserved in many species. Behavioral studies in humans and animals provide a necessary foundation to link the insights being obtained from human EEG and fMRI to those from animal neurophysiology. The aggregate of data resulting from multiple approaches across species has begun to clarify the neuronal bases of auditory restoration. Different types of neural responses supporting restoration have been found, supportive of multiple mechanisms working within a species. Yet a general principle has emerged that responses correlated with restoration mimic the response that would have been given to the uninterrupted sound of interest. Using the same technology to study different species will help us to better harness animal models of ‘auditory scene analysis’ to clarify the conserved neural mechanisms shaping the perceptual organization of sound and to advance strategies to improve hearing in natural environmental settings.

Research highlights

► Auditory perceptual restoration ability appears to be broadly conserved in animals. ► Single neuron response correlates of auditory restoration have been found. ► Human EEG and fMRI and animal electrophysiology show general correspondences. ► A simple principle can predict neural responses consistent with restoration.

Section snippets

The challenges of restoring masked or obliterated sensory input

Under natural listening conditions, there are many sound producing objects. This interferes with the ability to track sound emanating from a single source and to discriminate and identify features of that sound. Under these conditions we can consider the sound source and features we wish to follow as signal and sound emanating from other sources as ‘noise’. While sound location is one cue that can be used for source segregation, there is abundant evidence that under most conditions non-spatial

Do non-human animals experience auditory restoration?

What are the evolutionary origins of auditory restoration and exactly which species are susceptible to it? This is important to ask if we are to better understand the neural mechanisms underlying perceptual restoration. It seems obvious that the ability to fill-in incomplete information would be useful to animals, but until recently it was unclear if any animals besides humans experience this phenomenon or whether good animal models exist to study fill-in with techniques that are impractical

Insights from animal neurophysiology: restoration is related to both increases and decreases in firing rate

As is often the case, knowledge of the neurobiology underlying perception follows a growth in behavioral research, which establishes the necessary foundation for neurobiological study. As such there have been fewer neurophysiological recordings in the animal models of auditory restoration.

Schreiner investigated neuronal responses in the medial geniculate body (MGB) of the auditory thalamus of unanaesthetized guinea pigs while presenting sequentially alternating 100 ms broadband (0.1–22 kHz)

Insights from human EEG and fMRI: links from humans to other animals

Working with humans has the advantage that behaviorally humans can be tested much more flexibly. For example humans can readily report a percept and a confidence rating while physiological measurement is made. Also rather than studying small areas of the brain in detail as is usually done with animal electrophysiology, neuroimaging has the potential to show regional brain responses that may be overlooked in animal studies. Because of this it is important to keep in mind that the non-invasive

Neuronal principles for perceptual restoration

It seems unlikely that a single neuronal mechanism can support auditory restoration because (1) many different types of sounds need to be restored from many different potential occluders and (2) a diversity of neuronal response types and brain activity are related to restoration (e.g., theta band activity in EEG). Yet, Bregman (1990) predicted that neuronal responsiveness is maintained during continuity, which still resonates as a valid neuronal gestalt for perceptual restoration. Others have

A meeting of the human and non-human animal work and the path ahead

In conclusion, despite a long history of human behavior that has enhanced our understanding of perceptual restoration, understanding of the neurobiology underlying it has been slow to come about. Based on the use of natural response and psychophysical training paradigms, it is now clear that the perception of auditory restoration is far-reaching in animals, and that animal models can be used to probe the neurobiological mechanisms responsible for restoration. Single-neuron recordings in animals

Conflict of interest

The authors declare no competing financial interests.

Acknowledgements

We thank K. O’Connor for being a key contributor to our work together that is mentioned in this review and to J. Johnson, R. Lurz, and L. Riecke for comments on drafts of the manuscript. We also thank K. Vinnik and E. Balaban for valuable discussions and L. Riecke and E. Formisano for providing figures from their work. Supported by grants from Newcastle University, the McDonnell Foundation and the NIDCD (DC-02514).

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