Multifunctional facets of prefrontal oscillatory dynamics in support of perception and action

Abstract

This study aims to understand how oscillations of the prefrontal cortex lead to behavioral expression of higher cognitive function, as well as the specific mechanism that underpins it. Even though there has been considerable amount of understanding in the microscopic level (e.g., spiking) mechanism, there has been a lack of empirical findings that explain how prefrontal oscillations modify neural processing in meso- and macroscopic levels. Due to their direct linkage between large scale neural dynamics and cognitive processes which are innately emergent, studies on the influence of neural oscillations in meso- and macroscopic level explains the principle of behavior better than those of microscopic level. These studies have relied heavily on human participants to characterize the precise behavioral state of experimental subjects, where the use of invasive research procedures is severely restricted, rather than rodent models. As a result, establishing the causality of the role of prefrontal oscillations in changing neural processing in meso- and microscopic neuronal entities that directly represent higher cognitive functions become increasingly challenging. In this study, without relying on human or non-human primate subjects, I show how prefrontal oscillations modify neural information processing in meso- and macroscopic scale by overcoming the constraints of rodent model studies. In addition, I provide novel interpretations of the effect of prefrontal oscillations on cortical information, taking into consideration the information processing rules of the multilevel functional entities that comprise the nervous system. To this end, advanced methods for experimentation, measurements, and machine learning-based behavioral analyses were introduced, to observe the micro-states of mice which has non-uniformity by dissecting them in sub-second level, as well as through systematic quantitative EEG analysis. First, the role of prefrontal theta wave is to be investigated, in facilitating unidirectional relay of sensory information. Using visual Go/No-go task and behavioral analysis that assumes non-uniformity of sustained attention, I revealed that prefrontal theta inhibits endogenous brain activities in the visual cortex to promote sensory relaying in the occipital-prefrontal direction. Secondly, I introduced a predator threat situation in freely moving mice to study the link between behavior and prefrontal oscillations in a state of high ecological validity. Artificial intelligence and image processing techniques were used to dissect non-uniform behavioral states as microstates in sub-second units, and it was discovered that prefrontal oscillations of low- and high theta led to flexible transitions of behavior states through transient network compositions. Furthermore, by applying motion trajectory analysis, I found the role of prefrontal beta oscillations is a top-down gating of sensory information by silencing feedforward fast components in neural activities from the basolateral amygdala. Lastly, I introduced an example of rodent EEG database in a standardized format database, published with the core analysis scripts used for data analysis, supporting the open science movement triggered by replication crisis, especially in the human and primate model-based cognitive sciences community. Current study explains how the prefrontal oscillations affect the functional entities at the meso- and macroscopic level through specific examples: (1) facilitating relaying of sensory information, (2) flexible switching of neural circuits, and (3) selective gating. Furthermore, the significance of this study also stands at where it provides a steppingstone of translational research by using rodent model.