Information flows from hippocampus to auditory cortex during replay of verbal working memory items

Elife. 2022 Aug 12;11:e78677. doi: 10.7554/eLife.78677.

Abstract

The maintenance of items in working memory (WM) relies on a widespread network of cortical areas and hippocampus where synchronization between electrophysiological recordings reflects functional coupling. We investigated the direction of information flow between auditory cortex and hippocampus while participants heard and then mentally replayed strings of letters in WM by activating their phonological loop. We recorded local field potentials from the hippocampus, reconstructed beamforming sources of scalp EEG, and - additionally in four participants - recorded from subdural cortical electrodes. When analyzing Granger causality, the information flow was from auditory cortex to hippocampus with a peak in the [4 8] Hz range while participants heard the letters. This flow was subsequently reversed during maintenance while participants maintained the letters in memory. The functional interaction between hippocampus and the cortex and the reversal of information flow provide a physiological basis for the encoding of memory items and their active replay during maintenance.

Keywords: Granger causality; auditory cortex; computational biology; human; neuroscience; phase-locking value; systems biology; theta rhythm.

Plain language summary

Every day, the brain’s ability to temporarily store and recall information – called working memory – enables us to reason, solve complex problems or to speak. Holding pieces of information in working memory for short periods of times is a skill that relies on communication between neural circuits that span several areas of the brain. The hippocampus, a seahorse-shaped area at the centre of the brain, is well-known for its role in learning and memory. Less clear, however, is how brain regions that process sensory inputs, including visual stimuli and sounds, contribute to working memory. To investigate, Dimakopoulos et al. studied the flow of information between the hippocampus and the auditory cortex, which processes sound. To do so, various types of electrodes were placed on the scalp or surgically implanted in the brains of people with drug-resistant epilepsy. These electrodes measured the brain activity of participants as they read, heard and then mentally replayed strings of up to 8 letters. The electrical signals analysed reflected the flow of information between brain areas. When participants read and heard the sequence of letters, brain signals flowed from the auditory cortex to the hippocampus. The flow of electrical activity was reversed while participants recalled the letters. This pattern was found only in the left side of the brain, as expected for a language related task, and only if participants recalled the letters correctly. This work by Dimakopoulos et al. provides the first evidence of bidirectional communication between brain areas that are active when people memorise and recall information from their working memory. In doing so, it provides a physiological basis for how the brain encodes and replays information stored in working memory, which evidently relies on the interplay between the hippocampus and sensory cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Auditory Cortex*
  • Electroencephalography
  • Hippocampus / physiology
  • Humans
  • Memory, Short-Term / physiology

Grant support

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.