Human anterior insula signals salience and deviations from expectations via bursts of beta oscillations

Darrell Haufler, Omer Liran, Robert J. Buchanan, Denis Pare

Research output: Contribution to journalArticlepeer-review

Abstract

Functional imaging studies indicate that the insula encodes the salience of stimuli and deviations from expectations, signals that can mobilize cognitive resources and facilitate learning. However, there is no information about the physiological underpinnings of these phenomena beyond changing BOLD signals. To shed light on this question, we analyzed intracerebral local field potentials (LFPs) in five patients with epilepsy of both genders performing a virtual reality task that featured varying odds of monetary rewards and losses. Upon outcome disclosure, the anterior (but not the posterior) insula generated bursts of beta oscillations whose amplitudes were lower for neutral than positive and negative outcomes, consistent with a salience signal. Moreover, beta burst power was higher when outcomes deviated from expectations, whether the outcome was better or worse than expected, indicating that the insula provides an unsigned prediction error signal. Last, in relation to insular beta bursts, many higher-order cortical areas exhibited robust changes in LFP activity that ranged from spectrally nonspecific or differentiated increases in gamma power to bursts of beta activity that closely resembled the insular beta bursts themselves. Critically, the activity of these other cortical regions was more closely tied in time to insular bursts than task events, suggesting that they are associated with particularly significant cognitive phenomena. Overall, our findings suggest that the insula signals salience and prediction errors via amplitude modulations of beta bursts, which coincide with the near simultaneous recruitment of vast cortical territories.

Original languageEnglish (US)
Pages (from-to)160-180
Number of pages21
JournalJournal of neurophysiology
Volume128
Issue number1
DOIs
StatePublished - 2022

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Keywords

  • Beta
  • insula
  • oscillations
  • prediction error
  • salience

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