Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials

Learning to anticipate future states of the world based on statistical regularities in the environment is a key component of perception and is vital for the survival of many organisms. Such statistical learning and prediction are crucial for acquiring language and music appreciation. Importantly, le...

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Main Authors: Yonatan I. Fishman, Wei-Wei Lee, Elyse Sussman
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920309575
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author Yonatan I. Fishman
Wei-Wei Lee
Elyse Sussman
author_facet Yonatan I. Fishman
Wei-Wei Lee
Elyse Sussman
author_sort Yonatan I. Fishman
collection DOAJ
description Learning to anticipate future states of the world based on statistical regularities in the environment is a key component of perception and is vital for the survival of many organisms. Such statistical learning and prediction are crucial for acquiring language and music appreciation. Importantly, learned expectations can be implicitly derived from exposure to sensory input, without requiring explicit information regarding contingencies in the environment. Whereas many previous studies of statistical learning have demonstrated larger neuronal responses to unexpected versus expected stimuli, the neuronal bases of the expectations themselves remain poorly understood. Here we examined behavioral and neuronal signatures of learned expectancy via human scalp-recorded event-related brain potentials (ERPs). Participants were instructed to listen to a series of sounds and press a response button as quickly as possible upon hearing a target noise burst, which was either reliably or unreliably preceded by one of three pure tones in low-, mid-, and high-frequency ranges. Participants were not informed about the statistical contingencies between the preceding tone ‘cues’ and the target. Over the course of a stimulus block, participants responded more rapidly to reliably cued targets. This behavioral index of learned expectancy was paralleled by a negative ERP deflection, designated as a neuronal contingency response (CR), which occurred immediately prior to the onset of the target. The amplitude and latency of the CR were systematically modulated by the strength of the predictive relationship between the cue and the target. Re-averaging ERPs with respect to the latency of behavioral responses revealed no consistent relationship between the CR and the motor response, suggesting that the CR represents a neuronal signature of learned expectancy or anticipatory attention. Our results demonstrate that statistical regularities in an auditory input stream can be implicitly learned and exploited to influence behavior. Furthermore, we uncover a potential ‘prediction signal’ that reflects this fundamental learning process.
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spelling doaj.art-6a9f8fe5c92f46bdafda40aa001c14db2022-12-21T22:29:05ZengElsevierNeuroImage1095-95722021-01-01225117472Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentialsYonatan I. Fishman0Wei-Wei Lee1Elyse Sussman2Department of Neurology, Albert Einstein College of Medicine, United States; Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, United States; Corresponding author at: Albert Einstein College of Medicine, Neurology, 1410 Pelham Parkway, Bronx, Bronx, NY 10461, United States.Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, United StatesDominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, United StatesLearning to anticipate future states of the world based on statistical regularities in the environment is a key component of perception and is vital for the survival of many organisms. Such statistical learning and prediction are crucial for acquiring language and music appreciation. Importantly, learned expectations can be implicitly derived from exposure to sensory input, without requiring explicit information regarding contingencies in the environment. Whereas many previous studies of statistical learning have demonstrated larger neuronal responses to unexpected versus expected stimuli, the neuronal bases of the expectations themselves remain poorly understood. Here we examined behavioral and neuronal signatures of learned expectancy via human scalp-recorded event-related brain potentials (ERPs). Participants were instructed to listen to a series of sounds and press a response button as quickly as possible upon hearing a target noise burst, which was either reliably or unreliably preceded by one of three pure tones in low-, mid-, and high-frequency ranges. Participants were not informed about the statistical contingencies between the preceding tone ‘cues’ and the target. Over the course of a stimulus block, participants responded more rapidly to reliably cued targets. This behavioral index of learned expectancy was paralleled by a negative ERP deflection, designated as a neuronal contingency response (CR), which occurred immediately prior to the onset of the target. The amplitude and latency of the CR were systematically modulated by the strength of the predictive relationship between the cue and the target. Re-averaging ERPs with respect to the latency of behavioral responses revealed no consistent relationship between the CR and the motor response, suggesting that the CR represents a neuronal signature of learned expectancy or anticipatory attention. Our results demonstrate that statistical regularities in an auditory input stream can be implicitly learned and exploited to influence behavior. Furthermore, we uncover a potential ‘prediction signal’ that reflects this fundamental learning process.http://www.sciencedirect.com/science/article/pii/S1053811920309575PredictionStatistical learningExpectancyAuditory perceptionEEGContingent Negative Variation (CNV)
spellingShingle Yonatan I. Fishman
Wei-Wei Lee
Elyse Sussman
Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
NeuroImage
Prediction
Statistical learning
Expectancy
Auditory perception
EEG
Contingent Negative Variation (CNV)
title Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
title_full Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
title_fullStr Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
title_full_unstemmed Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
title_short Learning to predict: Neuronal signatures of auditory expectancy in human event-related potentials
title_sort learning to predict neuronal signatures of auditory expectancy in human event related potentials
topic Prediction
Statistical learning
Expectancy
Auditory perception
EEG
Contingent Negative Variation (CNV)
url http://www.sciencedirect.com/science/article/pii/S1053811920309575
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