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J Neurosci. 2018 Feb 7;38(6):1541-1557. doi: 10.1523/JNEUROSCI.1779-17.2017. Epub 2018 Jan 8.

Neural Integration of Stimulus History Underlies Prediction for Naturalistically Evolving Sequences.

Author information

1
National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892.
2
Neuroscience Institute, New York University Langone Medical Center, New York, New York 10016.
3
Universitary of Lyon, Ens de Lyon, University Claude Bernard, CNRS, Laboratoire de Physique, F-69342 Lyon, France.
4
Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neurocience and Human Behavior, University of California, Los Angeles, California 90095.
5
National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, and.
6
National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892, biyu.jade.he@gmail.com.
7
Departments of Neurology, Neuroscience, and Physiology, and Radiology, New York University Langone Medical Center, New York 10016.

Abstract

Forming valid predictions about the environment is crucial to survival. However, whether humans are able to form valid predictions about natural stimuli based on their temporal statistical regularities remains unknown. Here, we presented subjects with tone sequences with pitch fluctuations that, over time, capture long-range temporal dependence structures prevalent in natural stimuli. We found that subjects were able to exploit such naturalistic statistical regularities to make valid predictions about upcoming items in a sequence. Magnetoencephalography (MEG) recordings revealed that slow, arrhythmic cortical dynamics tracked the evolving pitch sequence over time such that neural activity at a given moment was influenced by the pitch of up to seven previous tones. Importantly, such history integration contained in neural activity predicted the expected pitch of the upcoming tone, providing a concrete computational mechanism for prediction. These results establish humans' ability to make valid predictions based on temporal regularities inherent in naturalistic stimuli and further reveal the neural mechanisms underlying such predictive computation.SIGNIFICANCE STATEMENT A fundamental question in neuroscience is how the brain predicts upcoming events in the environment. To date, this question has primarily been addressed in experiments using relatively simple stimulus sequences. Here, we studied predictive processing in the human brain using auditory tone sequences that exhibit temporal statistical regularities similar to those found in natural stimuli. We observed that humans are able to form valid predictions based on such complex temporal statistical regularities. We further show that neural response to a given tone in the sequence reflects integration over the preceding tone sequence and that this history dependence forms the foundation for prediction. These findings deepen our understanding of how humans form predictions in an ecologically valid environment.

KEYWORDS:

1/f activity; magnetoencephalography; naturalistic stimuli; predictive processing; scale-free dynamics

PMID:
29311143
PMCID:
PMC5815353
DOI:
10.1523/JNEUROSCI.1779-17.2017
[Indexed for MEDLINE]
Free PMC Article

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