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

• Published in: NeuroImage (Orlando, Fla.) Vol. 225; p. 117472
• Main Authors: Fishman, Yonatan I., Lee, Wei-Wei, Sussman, Elyse
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 15-01-2021; Elsevier Limited; Elsevier
• Subjects: Acoustic Stimulation; Adult; Attention; Auditory perception; Auditory Perception - physiology; Behavior; Brain - physiology; Contingent Negative Variation (CNV); Cues; EEG; Electroencephalography; Event-related potentials; Evoked Potentials - physiology; Evoked Potentials, Auditory - physiology; Expectancy; Female; Humans; Latency; Learning; Learning - physiology; Male; Medical screening; Music; Noise; Prediction; Scalp; Signatures; Statistical learning; Statistics; Contingent Negative Variation (CNV); Expectancy; Statistical learning; EEG; Prediction; Auditory perception
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2020.117472

•Event-related brain potentials and behavioral results demonstrate implicit learning of auditory statistical regularities.•A neuronal ‘prediction signal’ was associated with implicitly learned cue-target contingencies.•The ‘prediction signal’ was modulated by the strength of the cue-target relationship.•Neuronal signatures of learned expectancy were congruent with changes in reaction time.
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.