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Deviance Detection Based on Regularity Encoding Along the Auditory Hierarchy: Electrophysiological Evidence in Humans

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Abstract

Detection of changes in the acoustic environment is critical for survival, as it prevents missing potentially relevant events outside the focus of attention. In humans, deviance detection based on acoustic regularity encoding has been associated with a brain response derived from the human EEG, the mismatch negativity (MMN) auditory evoked potential, peaking at about 100–200 ms from deviance onset. By its long latency and cerebral generators, the cortical nature of both the processes of regularity encoding and deviance detection has been assumed. Yet, intracellular, extracellular, single-unit and local-field potential recordings in rats and cats have shown much earlier (circa 20–30 ms) and hierarchically lower (primary auditory cortex, medial geniculate body, inferior colliculus) deviance-related responses. Here, we review the recent evidence obtained with the complex auditory brainstem response (cABR), the middle latency response (MLR) and magnetoencephalography (MEG) demonstrating that human auditory deviance detection based on regularity encoding—rather than on refractoriness—occurs at latencies and in neural networks comparable to those revealed in animals. Specifically, encoding of simple acoustic-feature regularities and detection of corresponding deviance, such as an infrequent change in frequency or location, occur in the latency range of the MLR, in separate auditory cortical regions from those generating the MMN, and even at the level of human auditory brainstem. In contrast, violations of more complex regularities, such as those defined by the alternation of two different tones or by feature conjunctions (i.e., frequency and location) fail to elicit MLR correlates but elicit sizable MMNs. Altogether, these findings support the emerging view that deviance detection is a basic principle of the functional organization of the auditory system, and that regularity encoding and deviance detection is organized in ascending levels of complexity along the auditory pathway expanding from the brainstem up to higher-order areas of the cerebral cortex.

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Acknowledgments

This work was supported by the Spanish Ministry of Economy and Knowledge: Project PSI2012-37174, Programa Euroinvestigación-EUI2009-04086 awarded to the ERANET-NEURON Project PANS, and Consolider-Ingenio 2010 program (CDS2007-00012). Funds were also received from a grant from the Catalan Government (SGR2009-11) and the ICREA Academia Distinguished Professorship awarded to Carles Escera.

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  1. Institute for Brain, Cognition and Behavior (IR3C), University of Barcelona, Passeig Vall d’Hebron 171, 08035, Barcelona, Catalonia, Spain

    Carles Escera, Sumie Leung & Sabine Grimm

  2. Cognitive Neuroscience Research Group, Department of Psychiatry and Clinical Psychobiology, University of Barcelona, Passeig Vall d’Hebron 171, 08035, Barcelona, Catalonia, Spain

    Carles Escera, Sumie Leung & Sabine Grimm

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  1. Carles Escera
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Correspondence to Carles Escera.

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This is one of several papers published together in Brain Topography in the “Special Issue: Mismatch Negativity”.

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Escera, C., Leung, S. & Grimm, S. Deviance Detection Based on Regularity Encoding Along the Auditory Hierarchy: Electrophysiological Evidence in Humans. Brain Topogr 27, 527–538 (2014). https://doi.org/10.1007/s10548-013-0328-4

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