Age-related double dissociation of fast and slow theta oscillations in children and adolescents

• In Event: Poster Session 14
  In Poster Session: PS 14 Topic - Biological Processes: Neuroscience and Genetics

Abstract

Neuronal oscillations are ubiquitous and associated with processes ranging from physiological to cognitive to pathological. Indeed, lack of activity in the electroencephalogram (EEG) signifies brain death. These periodic rhythms change considerably during development, making understanding their development fundamental to understanding the development of the brain. Since the first human EEG in 1929 (Berger, 1930), researchers have focused on the dominant alpha rhythm, defined by a frequency of 8-12 Hz in adults. Alpha oscillations emerge spontaneously during infancy at 3-4 Hz, speed up to 5-7 Hz by the end of the first year of life, and reach adult-level frequencies around 12 years of age (e.g., Lindsley, 1939). However, scalp EEG does not access medial brain areas directly and offers low spatial resolution of the lateral areas it does access. Noninvasive EEG therefore offers a limited window into brain development and, as we consider here, the development of cognitive processes such as declarative memory which rely on the medial temporal lobe (MTL) and its connections to specific lateral prefrontal (PFC) areas (Ofen et al., 2019). To circumvent this issue, we capitalized on a unique opportunity to record EEG directly from the brains of pediatric neurosurgical patients undergoing invasive clinical monitoring for seizure management. With appropriate cleaning to remove data related to seizures, these data represent healthy neural activity (Rossini et al., 2017).

In this study, 21 children and adolescents (5.9-20.5 years) undergoing direct cortical monitoring (i.e., electrocorticography [ECoG]) attended to visual scenes in preparation for a memory recognition test. We isolated ECoG signals from 80 channels in MTL and 357 channels in PFC, subdivided into inferior, middle, and superior frontal gyri based on individual neuroanatomy. We focused on theta rhythms, which are defined by a frequency of 3-8 Hz and have been consistently linked to memory processes in the MTL of adults as well as animal models (e.g., Johnson et al., 2020). After disentangling oscillatory components from aperiodic 1/f activity (e.g., Wen & Liu, 2016), we observed frequency shifts in rhythms at both ends of the theta band. A faster rhythm was detected ~7 Hz which sped up with age and a slower rhythm was detected ~3 Hz which slowed down with age. This age-related double dissociation was observed in MTL and throughout PFC (all linear mixed-effects model p’s < 0.012). With these results, we show for the first time that: (1) recent findings of fast and slow theta rhythms in the adult MTL (Choi et al., 2020; Goyal et al., 2020) extend to children; (2) both theta rhythms are also evident in PFC; and (3) development is associated with the functional differentiation of theta oscillations. Further analyses show that both theta oscillations support MTL-PFC functional connectivity patterns predictive of subsequent memory formation, suggesting that the functional differentiation of theta oscillations relates to the development of declarative memory.

Authors

• Elizabeth Johnson, Northwestern University
  Presenting Author

• Qin Yin, Wayne State University
  Non-Presenting Author

• Lingfei Tang, Wayne State University
  Non-Presenting Author

• Eishi Asano, Wayne State University School of Medicine
  Non-Presenting Author

• Noa Ofen, Wayne State University
  Non-Presenting Author