Processing of complex stimuli and natural scenes in the auditory cortex

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Neuronal responses in auditory cortex show a fascinating mixture of characteristics that span the range from almost perfect copies of physical aspects of the stimuli to extremely complex context-dependent responses. Fast, highly stimulus-specific adaptation and slower plastic mechanisms work together to constantly adjust neuronal response properties to the statistics of the auditory scene. Evidence with converging implications suggests that the neuronal activity in primary auditory cortex represents sounds in terms of auditory objects rather than in terms of invariant acoustic features.

Introduction

Research into signal coding in primary auditory cortex (A1) has enjoyed renewed popularity in recent years. All modern methodologies, including new slice preparations for studying thalamo–cortical interactions [1], intracellular and extracellular single neuron recordings 2., 3.••, 4.••, evoked electrical and magnetic fields (EEG and MEG) 5., 6.•, and functional magnetic resonance imaging (fMRI) 7., 8., are being applied to this system in a variety of model animals, including rodents, bats, cats, primates, and humans.

Despite this accumulation of information, the nature of the representation of complex sounds in A1 remains the subject of heated debate. This is not due to a lack of data, but rather because of the fact that the data are often contradictory. Whereas some studies emphasize a relatively simple cortical representation, other studies show a large degree of complexity in the neuronal responses.

Here, I review evidence that indicates that simplicity and complexity co-exist in A1. Evidence with converging implications suggests that the co-existence of simplicity and complexity in A1 is due to its participation in processes that are often implicitly assigned to higher brain areas. In particular, I review evidence that suggests the involvement of auditory cortex in processes such as the on-line extraction of statistical regularities from the auditory scene and the organization of the auditory scene in terms of auditory objects.

Section snippets

Precise and imprecise temporal coding

One of the complexities in auditory cortex is the interplay among multiple time scales that determine the neural responses. For example, cortical neurons respond to some auditory events with stereotypical response bursts at a fixed latency (‘locking’). The variance of the latency of such bursts might be similar to that of peripheral neurons. However, the same neurons may show sluggish responses to other features of the sounds.

Temporal coding is usually tested using repetitive stimuli, such as

Feature detection or something else?

It seems that depending upon the circumstances, a cortical neuron can choose to be sluggish or precise, linear or non-linear. Thus, the feature sensitivity of a neuron, as determined, for example, by its STRF, cannot be used as an invariant essential characterization of its responses. The multiple time scales at which cortical neurons process sounds provide another argument against a pure role in feature-detection for auditory cortex neurons [25]. Feature detectors are expected to be sensitive

Adaptation and plasticity

The plastic capabilities of auditory cortex have been studied in several preparations on many time scales. Significant changes in electrical and magnetic brain potentials (EEG and MEG) occur during training for the performance of tasks such as the perception of virtual pitch [5] and fine pitch discrimination [37]. Even simple exposure to different auditory environments can substantially change auditory cortical organization and responses: thus, raising rats in an enriched environment increases

Auditory scene analysis in auditory cortex

Several recent studies, using a variety of techniques, suggest a role for auditory cortex in segregation and grouping of sound components. For example, at the brain potential level, Dyson and Alain [50] reported that the amplitude of the mid-latency potentials increased when a harmonic was mistuned, potentially creating two auditory objects instead of one. Furthermore, the enhanced amplitude was correlated with an increased likelihood of reporting two concurrent auditory objects. Krumbholz et al

Speculative synthesis and conclusions

Most of the interesting auditory features might already be extracted from the incoming sounds by the level of the IC, which should therefore be considered as the auditory analog of the primary visual cortex (V1). The role of auditory cortex is to organize these features into auditory objects (Figure 1). To do that, auditory cortex has to use temporal and spectral context at several time scales. The large adaptive and plastic capacity of auditory cortex is used to tune the neural circuits to the

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Supported by grants from the Israeli Science Foundation (ISF), the German-Israeli Foundation (GIF) and the Volkswagenstiftung.

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