Meso-microscale physiology and dynamics of slow network fluctuations

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ABSTRACT: Neural networks orchestrate behavior across multiple timescales and are disordered in numerous developmental, neurological, and psychiatric disorders. Here we use intracranial EEG recording in humans (iEEG) to address the role of slow brain network fluctuations (SBNFs) and local cortical activation in the neural circuits supporting external attention and attention to our internal thoughts. Notably, attention to inner thoughts occupies up to fifty percent of our awake time but has received considerably less research focus which we will address in the Conte Center. We focus on differential interactions between the default mode network (DMN) and the fronto-parietal attention networks (FPCN) in support of these two core attention states. Local neural activation is measured with broadband high frequency activity (BHA; 70-200 Hz) and single-unit activity (SUA). Inter-areal network interactions are assessed using connectivity metrics including phase slope index, single- trial HFA onsets, Granger causality, directional phase amplitude coupling, representational similarity and mutual information. To examine slow fluctuations of internally versus externally directed attention across temporal and cognitive scales, we start with well-controlled paradigms and systematically increase experimental naturalism across three AIMS. AIM 1 employs structured tasks including switching between external and internal attention states with a focus on the role of anterior insula and posterior cingulate in switching. An intermodal auditory-visual attention task probes attention and lapses. In another condition we deliver the same intermodal streams while the subject paces and slows down breaths to increase vagal afferent firing, providing iEEG evidence of interoception and its effects on attention networks. AIM 2 uses a more naturalistic paradigm entailing passive viewing of movies. EOMs, alpha oscillations, BHA and pupillometry indexes drifts away from active attention to internal thought. We use a post-movie recognition task to confirm lapses of external attention to the movies and assess the changes in the properties of interactions between the DMN and FPCNa and FPCNb networks. AIM 3 uses experience sampling coupled with continuous iEEG recording across multiple days. Subjects are queried about their internal mental state (on- task: reading a book, talking to a family member or health provider) or off-task and mind-wandering as further determined by the behavioral metrics also used in P1. This task provides a powerful test of the networks supporting external versus internal attention in the most naturalistic environment one can achieve in an epilepsy monitoring unit. During internal thought we assess freely moving thoughts that drift from one topic to another, deliberately constrained thoughts focusing on an overarching goal, and automatically constrained thoughts drawn to personally or affectively salient topics. Our findings coupled with the EEG and fMRI results in P1 and the macaque data in P3 will improve our understanding of how SBNFs underpin and support both normal cognition and disordered attention in neuropsychiatric disorders.