Low-frequency cortical oscillations entrain to sub-threshold rhythmic auditory stimuli

Sanne Ten Oever, Charles E Schroeder, David Poeppel, Nienke van Atteveldt, Ashesh D Mehta, Pierre Mégevand, David M Groppe, Elana Zion-Golumbic

Research output: Contribution to JournalArticleAcademicpeer-review

10 Downloads (Pure)

Abstract

Many environmental stimuli contain temporal regularities, a feature which can help predict forthcoming input. Phase-locking (entrainment) of ongoing low-frequency neuronal oscillations to rhythmic stimuli is proposed as a potential mechanism for enhancing neuronal responses and perceptual sensitivity, by aligning high-excitability phases to events within a stimulus stream. Previous experiments show that rhythmic structure has a behavioral benefit even when the rhythm itself is below perceptual detection thresholds (Ten Oever et al., 2014). It is not known whether this "inaudible" rhythmic sound stream also induces entrainment. Here we tested this hypothesis using magnetoencephalography (MEG) and electrocorticography (ECoG) in humans to record changes in neuronal activity as subthreshold rhythmic stimuli gradually became audible. We found that significant phase-locking to the rhythmic sounds preceded participants' detection of them. Moreover, no significant auditory-evoked responses accompanied this pre-threshold entrainment. These auditory-evoked responses, distinguished by robust, broad-band increases in inter-trial coherence (ITC), only appeared after sounds were reported as audible. Taken together with the reduced perceptual thresholds observed for rhythmic sequences, these findings support the proposition that entrainment of low-frequency oscillations serves a mechanistic role in enhancing perceptual sensitivity for temporally-predictive sounds. This framework has broad implications for understanding the neural mechanisms involved in generating temporal predictions and their relevance for perception, attention, and awareness.SIGNIFICANCE STATEMENTThe environment is full of rhythmically structured signals that the nervous system can exploit for information processing. Thus it is important to understand how the brain processes such temporally structured, regular features of external stimuli. Here we report the alignment of slowly fluctuating oscillatory brain activity to external rhythmic structure prior to its behavioral detection. These results indicate that phase alignment is a general mechanism of the brain to process rhythmic structure, and can occur without the perceptual detection of this temporal structure.

Original languageEnglish
Pages (from-to)4903-4912
Number of pages10
JournalThe Journal of Neuroscience
Volume37
Issue number19
Early online date14 Apr 2017
DOIs
Publication statusPublished - 10 May 2017

Funding

This study was supported by Dutch Organization for Scientific Research Grant 406-11-068; the I-CORE Program of the Planning and Budgeting Committee; Israel Science Foundation Grant 51/11; NIH Grants MH103814, EY024776, and R01DC05660; Swiss National Science Foundation Grant 148388; and the Page and Otto Marx Jr. Foundation.

FundersFunder number
Page and Otto Marx Jr
National Institutes of HealthMH103814, R01DC05660
National Eye InstituteR21EY024776
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung148388
Nederlandse Organisatie voor Wetenschappelijk Onderzoek406-11-068
Israel Science Foundation51/11
Planning and Budgeting Committee of the Council for Higher Education of Israel

    Keywords

    • Journal Article

    Fingerprint

    Dive into the research topics of 'Low-frequency cortical oscillations entrain to sub-threshold rhythmic auditory stimuli'. Together they form a unique fingerprint.

    Cite this