Dynamic coordination of neuronal circuits through inter-areal oscillatory synchronization

A central question in neuroscience is how does the brain accomplish context-sensitive computation? A well-established example of context-sensitive computation is visual selective attention, which involves enhancing some neuronal representations relative to others such that behaviorally relevant stimuli are preferentially processed. This cognitive computation most likely relies on a dynamic coordination of multiple, spatially-distributed neuronal circuits. This dissertation pursues the hypothesis that neuronal oscillations are intimately involved in this context-sensitive computation, by dynamically coordinating the activity between and within neuronal circuits through synchronization at distinct frequencies. In Chapter 1, I review the dynamic coordination problem and the existing evidence for oscillations as a mechanism thereof. In Chapter 2, I summarize the foundational concepts for the methods used in this dissertation to quantify inter-areal oscillatory synchronization. In Chapter 3, I describe how these methods were applied to high-density electrocorticography recordings from awake-behaving monkeys, and report large-scale networks of oscillatory synchronization and their modulation by selective attention. In Chapter 4, I describe how the hierarchical interactions between multiple areas of the visual cortex are revealed in functional data by showing that beta frequency rhythms flow in the top-down direction, and gamma frequency rhythms flow in the bottom-up direction. Furthermore, these counter-streaming directed influences define a functional hierarchy of the visual cortex which is highly similar to anatomy-based hierarchies. In Chapter 5, I describe an analysis of the anatomy and physiology of the underlying circuits which might have generated these structured patterns of oscillatory synchronization. The empirically observed circuit is compared to the theoretically predicted circuit implied by predictive coding theory. This analysis converges on the notion that some aspects of cortical circuitry and physiology are canonical, and that these circuits would be capable of implementing predictive coding through feedforward and feedback message passing amongst multiple hierarchically deployed canonical microcircuits. In Chapter 6, the canonical microcircuit model from Chapter 5 is used to model observed oscillatory synchronization patterns between two hierarchically-separated visual cortical areas. In Chapter 7, I consider whether oscillatory interactions are emergent properties of the cortex, or whether they are inherited from pre-cortical structures. Finally, in Chapter 8, I summarize the findings and consider challenges to the framework of dynamic coordination through oscillations.