Task-Evoked Functional Connectivity Does Not Explain Functional Connectivity Differences Between Rest and Task Conditions

Abstract

1During complex tasks, patterns of functional connectivity (FC) differ from those in the 2 resting state. What accounts for such differences remains unclear. Brain activity during a task 3 reflects an unknown mixture of spontaneous activity and task-evoked responses. The difference 4 in FC between a task state and resting state may reflect not only task-evoked connectivity, but 5 also changes in spontaneously emerging networks. Here, we characterized the difference in 6 apparent functional connectivity between the resting state and when human subjects were 7 watching a naturalistic movie. Such differences were marginally (3-15%) explained by the task-8 evoked networks directly involved in processing the movie content, but mostly attributable to 9 changes in spontaneous networks driven by ongoing activity during the task. The execution of 10 the task reduced the correlations in ongoing activity among different cortical networks, especially 11 between the visual and non-visual sensory cortices. Our results suggest that the interaction 12 between spontaneous and task-evoked activities is not mutually independent or linearly additive, 13 and that engaging in a task may suppress ongoing activity.

Non-additive activity modulation during a decision making task involving tactic selection

“…This means that the activity evoked by task or stimulus is assumed to superpose in a merely additive way on the ongoing spontaneous activity level. However, the generality of such a model of superposition or additive rest-stimulus interaction (Northoff et al 2010) has recently been put into doubt (He 2013;Huang et al 2017;Ding and Simon 2014;Ponce-Alvarez et al 2015;Lynch et al 2018;Wainio-Theberge et al 2021). Brain imaging studies on the regional level of neural activity demonstrated non-additive interaction with higher prestimulus activity level leading to lower (rather than higher) post-stimulus activity changes, and vice-versa (He 2013;Huang et al 2017;Ponce-Alvarez et al 2015;Lynch et al 2018;Cole et al 2016;He 2013).…”

“…However, the generality of such a model of superposition or additive rest-stimulus interaction (Northoff et al 2010) has recently been put into doubt (He 2013;Huang et al 2017;Ding and Simon 2014;Ponce-Alvarez et al 2015;Lynch et al 2018;Wainio-Theberge et al 2021). Brain imaging studies on the regional level of neural activity demonstrated non-additive interaction with higher prestimulus activity level leading to lower (rather than higher) post-stimulus activity changes, and vice-versa (He 2013;Huang et al 2017;Ponce-Alvarez et al 2015;Lynch et al 2018;Cole et al 2016;He 2013). The central role of prestimulus activity has also been demonstrated on the cellular level in rats (Haslinger et al 2006;Kisley and Gerstein 1999;Curto et al 2009) and mice (Llinás et al 2002;Guo et al 2015;Pachitariu et al 2015), and monkeys (van Vugt et al 2018).…”

How Tasks Change Whole-Brain Functional Organization to Reveal Brain-Phenotype Relationships

“…Although some have raised concerns that inadequate removal of task-evoked activation from node time courses may yield spurious patterns of FC (Cole et al, 2019), others have demonstrated that task-evoked activation and task-induced changes in FC can be cleanly dissociated (Di and Biswal, 2019) and contain complementary information about task performance (Tsvetanov et al, 2018), even when task-evoked activation is not removed from the blood-oxygen-level-dependent (BOLD) signal (Kieliba et al, 2019). Further, task-evoked FC (that is, task-induced changes in FC attributable to task-evoked activity) explains relatively little of the total task-induced change in FC (Lynch et al, 2018).…”

How tasks change whole-brain functional organization to reveal brain-phenotype relationships

“…In particular, the question of whether these changes reflect task-evoked activation, changes in neural interaction, or some combination of the two has received substantial attention. While some have raised concerns that inadequate removal of task-evoked activation from node time courses may yield spurious patterns of FC (Cole et al, 2019), others have demonstrated that task-evoked activation and task-induced changes in FC can be cleanly dissociated (Di & Biswal, 2018), even when task-evoked activation is not removed from the BOLD signal (Kieliba et al, 2018), and that task-evoked FC (that is, task-induced changes in FC attributable to task-evoked activity) explains relatively little of the total task-induced change in FC (Lynch et al, 2018).…”