Neural Integration of Stimulus History Underlies Prediction for Naturalistically Evolving Sequences

• Published in: The Journal of neuroscience Vol. 38; no. 6; pp. 1541 - 1557
• Main Authors: Maniscalco, Brian, Lee, Jennifer L., Abry, Patrice, Lin, Amy, Holroyd, Tom, He, Biyu J.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 07.02.2018
• Subjects: Acoustic Stimulation; Adult; Algorithms; Anticipation, Psychological - physiology; Auditory Perception - physiology; Brain; Computational neuroscience; Cortex; Evolution; Female; Frequency; Humans; Integration; Magnetoencephalography; Male; Nerve Net - physiology; Nervous system; Pitch; Pitch Perception - physiology; Predictions; Psychomotor Performance - physiology; Statistics; Stimuli; Time dependence; Variations; Young Adult; naturalistic stimuli; predictive processing; scale-free dynamics; 1/f activity; magnetoencephalography
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.1779-17.2017

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.