Dissociable oscillatory theta signatures of memory formation in the developing brain

Elizabeth L. Johnson*, Qin Yin, Nolan B. O'Hara, Lingfei Tang, Jeong Won Jeong, Eishi Asano, Noa Ofen

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Understanding complex human brain functions is critically informed by studying such functions during development. Here, we addressed a major gap in models of human memory by leveraging rare direct electrophysiological recordings from children and adolescents. Specifically, memory relies on interactions between the medial temporal lobe (MTL) and prefrontal cortex (PFC), and the maturation of these interactions is posited to play a key role in supporting memory development. To understand the nature of MTL-PFC interactions, we examined subdural recordings from MTL and PFC in 21 neurosurgical patients aged 5.9–20.5 years as they performed an established scene memory task. We determined signatures of memory formation by comparing the study of subsequently recognized to forgotten scenes in single trials. Results establish that MTL and PFC interact via two distinct theta mechanisms, an ∼3-Hz oscillation that supports amplitude coupling and slows down with age and an ∼7-Hz oscillation that supports phase coupling and speeds up with age. Slow and fast theta interactions immediately preceding scene onset further explained age-related differences in recognition performance. Last, with additional diffusion imaging data, we linked both functional mechanisms to the structural maturation of the cingulum tract. Our findings establish system-level dynamics of memory formation and suggest that MTL and PFC interact via increasingly dissociable mechanisms as memory improves across development.

Original languageEnglish (US)
Pages (from-to)1457-1469.e4
JournalCurrent Biology
Volume32
Issue number7
DOIs
StatePublished - Apr 11 2022

Keywords

  • brain development
  • cognitive development
  • diffusion tractography
  • electrocorticography
  • episodic memory
  • medial temporal lobe
  • prefrontal cortex
  • theta oscillations

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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