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Pupil-linked phasic arousal evoked by violation but not emergence of regularity within rapid sound sequences

Sijia Zhao,M. Chait,F. Dick,P. Dayan,S. Furukawa,Hsin-I Liao

Published 2019 in Nature Communications

ABSTRACT

The ability to track the statistics of our surroundings is a key computational challenge. A prominent theory proposes that the brain monitors for unexpected uncertainty – events which deviate substantially from model predictions, indicating model failure. Norepinephrine is thought to play a key role in this process by serving as an interrupt signal, initiating model-resetting. However, evidence is from paradigms where participants actively monitored stimulus statistics. To determine whether Norepinephrine routinely reports the statistical structure of our surroundings, even when not behaviourally relevant, we used rapid tone-pip sequences that contained salient pattern-changes associated with abrupt structural violations vs. emergence of regular structure. Phasic pupil dilations (PDR) were monitored to assess Norepinephrine. We reveal a remarkable specificity: When not behaviourally relevant, only abrupt structural violations evoke a PDR. The results demonstrate that Norepinephrine tracks unexpected uncertainty on rapid time scales relevant to sensory signals. The neurotransmitter Norepinephrine (NE) has been implicated in coding surprise during decision making. Here, the authors demonstrate that this extends to sensory processing: NE release is specific to unexpected events even on extremely rapid time scales and without explicit tracking of probability.

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