Human Pavlovian fear conditioning conforms to probabilistic learning

• Published in: PLoS computational biology Vol. 14; no. 8; p. e1006243
• Main Authors: Tzovara, Athina, Korn, Christoph W., Bach, Dominik R.
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 31.08.2018; Public Library of Science (PLoS)
• Subjects: Autonomic Nervous System - physiology; Biology and Life Sciences; Conditioning, Classical - physiology; Cues; Fear - physiology; Humans; Learning - physiology; Machine Learning; Models, Theoretical; Physical Sciences; Probability Learning; Research and Analysis Methods; Social Sciences
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1006243

Learning to predict threat from environmental cues is a fundamental skill in changing environments. This aversive learning process is exemplified by Pavlovian threat conditioning. Despite a plethora of studies on the neural mechanisms supporting the formation of associations between neutral and aversive events, our computational understanding of this process is fragmented. Importantly, different computational models give rise to different and partly opposing predictions for the trial-by-trial dynamics of learning, for example expressed in the activity of the autonomic nervous system (ANS). Here, we investigate human ANS responses to conditioned stimuli during Pavlovian fear conditioning. To obtain precise, trial-by-trial, single-subject estimates of ANS responses, we build on a statistical framework for psychophysiological modelling. We then consider previously proposed non-probabilistic models, a simple probabilistic model, and non-learning models, as well as different observation functions to link learning models with ANS activity. Across three experiments, and both for skin conductance (SCR) and pupil size responses (PSR), a probabilistic learning model best explains ANS responses. Notably, SCR and PSR reflect different quantities of the same model: SCR track a mixture of expected outcome and uncertainty, while PSR track expected outcome alone. In summary, by combining psychophysiological modelling with computational learning theory, we provide systematic evidence that the formation and maintenance of Pavlovian threat predictions in humans may rely on probabilistic inference and includes estimation of uncertainty. This could inform theories of neural implementation of aversive learning.