What Can iEEG Inform Us About Mechanisms of Spontaneous Behavior?

Abstract

While controlled experiments form the core of human brain researcha fundamental, yet far less studied, domain concerns the neuronal mechanism underlying freely-generated, spontaneous behavior. Intracranial recordings in conscious human patients offer an invaluable window into this question. Here we review relevant iEEG findings highlighting a universal mechanism underlying human free behavior: internally generated ultra-slow fluctuations in neuronal activity. These spontaneous firing dynamics are ubiquitous across the brain and appear at various scalesfrom functionally-specialized local subpopulations, to brain wide networks. Crucially, signatures of these slow fluctuations appear in every free behavior studied so far. Focusing on free recall as a paradigmatic example, we demonstrate that spontaneous activity fluctuationsmanifested as slow anticipatory waves in cortico-hippocampal circuitstend to precede spontaneous recollections by 1-2 seconds. Moreover, when patients attempt to constrain their spontaneous recollections to a particular category, intracranial recordings in the cortex reveal a category-specific "baseline shift", i.e., steady enhancement in the excitability of neuronal populations encoding the targeted category. Such top-down modulation can bias the free recall process by pushing the spontaneous fluctuations of the relevant neuronal subpopulations closer to the behavioral threshold. Along with evidence derived from fMRI studies, these iEEG experiments demonstrate that slow spontaneous fluctuations within the appropriate brain circuits may serve as a driving force behind the emergence of spontaneous thoughts and free human behavior.