Resting state fluctuations underlie free and creative verbal behaviors in the human brain

Abstract

Internally generated (free) ideas and creative thoughts constitute a fundamentally important aspect of the human experience, yet the neuronal mechanism driving these behaviors remains elusive. Here we examined the hypothesis that the common mechanism underlying free verbal behaviors is the ultra-slow activity fluctuations (termed "resting state fluctuations") that emerge spontaneously in the human brain.In our experiment, participants were asked to perform three voluntary verbal tasks: a verbal fluency task, a verbal creativity task (alternative uses of everyday objects) and a divergent thinking task (instances of common concepts), during fMRI scanning. BOLD-activity during these tasks was contrasted with a controldeterministic verbal task, in which the behavior was fully determined by external stimuli. Our results reveal that in all three voluntary tasks, the verbal-generation responses displayed a gradual anticipatory buildup that preceded the deterministic control-related responses by ~2 seconds. Importantly, variance analysis ruled out a time-jittered step-function response confound. Critically, the waveforms of the anticipatory buildups, as reflected in their time-frequency dynamics, were significantly correlated to the dynamics of resting state fluctuations, measured during a rest period prior to the tasks. Specifically, the amplitude of low frequency fluctuations (fALFF) of the resting state time-course and the voluntary verbal responses in the left inferior frontal gyrus (LH IFG), a central hub engaged in these tasks, were correlated across individual participants. This correlation was not a general BOLD-related or verbal-response related result, as it was not found during the externally-determined verbal control condition. Furthermore, it was specific to brain regions known to be involved in language production. These results indicate that the slow buildup preceding voluntary behaviors is linked to resting state fluctuations. Thus, these ubiquitous brain fluctuations may constitute a common neural mechanism underlying the generation of free and creative behaviors in the human brain.

The default network is causally linked to creative thinking

“…Interestingly, this finding is in line with our results demonstrating reduced creative fluency with DCS of left hemisphere DN and no change in originality, further suggesting a role for right hemisphere DN in original thinking. It should be noted that verbal and creative fluency are well correlated, and may partially overlap in function [34,35]. However, in all participating subjects, the cortex exposed during surgery was thoroughly mapped for language functions (stimulated systematically while evaluating for naming, comprehension, and free speech).…”

Modulation of proximity to criticality enhances slow activity fluctuations during free recall

“…As outlined in the introduction -numerous studies have revealed that these fluctuations are organized along highly complex but informative connectivity patterns (Fox et al, 2006;Fox & Raichle, 2007;Sadaghiani & Kleinschmidt, 2013;Strappini et al, 2019) suggested to be related to cognitive habits, traits and pathologies (Eldar et al, 2013;Hahamy et al, 2021;. Recently we have proposed (Broday-Dvir & Malach, 2021;Norman et al, 2017;Norman & Malach, 2022) that these spontaneous fluctuations constitute a universal driver of self-generated, voluntary and creative behaviors.…”

“…They have also been linked to other spontaneous behavioral manifestations such as spontaneous fluctuations in pupil diameter (Yellin et al, 2015) and spontaneous eyedrifts (Ramot et al, 2011). Recently, we have demonstrated a direct link between the spontaneous activity fluctuations and free and creative verbal behaviors (Broday-Dvir & Malach, 2021).…”

Pupil dilations prior to freely timed actions reflect the reported timing of conscious intention

“…The hypothesis that APDs reflect the "switch into awareness" across different types of spontaneous behaviors is further evidenced by findings that conscious decisions, but not the actions that express those decisions, are accompanied by pupil dilations 27 . Notably, similar slow-ramping buildups of neural activity precede other types of spontaneous behavior, including creative idea generation 70 , eureka moments during problem solving 71 , and free recall 69,72 , which may reflect spontaneous fluctuations that trigger a thought or action upon crossing a threshold 39,42 . The similarities between volition and other spontaneous behavior are striking and, we think, deserve further exploration.…”