A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks

Abstract

Cognitively demanding tasks that evoke activation in the brain's central-executive network (CEN) have been consistently shown to evoke decreased activation (deactivation) in the default-mode network (DMN). The neural mechanisms underlying this switch between activation and deactivation of large-scale brain networks remain completely unknown. Here, we use functional magnetic resonance imaging (fMRI) to investigate the mechanisms underlying switching of brain networks in three different experiments. We first examined this switching process in an auditory event segmentation task. We observed significant activation of the CEN and deactivation of the DMN, along with activation of a third network comprising the right fronto-insular cortex (rFIC) and anterior cingulate cortex (ACC), when participants perceived salient auditory event boundaries. Using chronometric techniques and Granger causality analysis, we show that the rFIC-ACC network, and the rFIC, in particular, plays a critical and causal role in switching between the CEN and the DMN. We replicated this causal connectivity pattern in two additional experiments: (i) a visual attention ''oddball'' task and (ii) a task-free resting state. These results indicate that the rFIC is likely to play a major role in switching between distinct brain networks across task paradigms and stimulus modalities. Our findings have important implications for a unified view of network mechanisms underlying both exogenous and endogenous cognitive control.brain networks ͉ cognitive control ͉ insula ͉ attention ͉ prefrontal cortex O ne distinguishing feature of the human brain, compared with brains lower on the phylogenetic ladder, is the amount of cognitive control available for selecting, switching, and attending to salient events in the environment. Recent research suggests that the human brain is intrinsically organized into distinct functional networks that support these processes (1-4). Analysis of resting-state functional connectivity, using both model-based and model-free approaches, has suggested the existence of at least three canonical networks: (i) a centralexecutive network (CEN), whose key nodes include the dorsolateral prefrontal cortex (DLPFC), and posterior parietal cortex (PPC); (ii) the default-mode network (DMN), which includes the ventromedial prefrontal cortex (VMPFC) and posterior cingulate cortex (PCC); and (iii) a salience network (SN), which includes the ventrolateral prefrontal cortex (VLPFC) and anterior insula (jointly referred to as the fronto-insular cortex; FIC) and the anterior cingulate cortex (ACC) (1, 2, 4, 5). During the performance of cognitively demanding tasks, the CEN and SN typically show increases in activation whereas the DMN shows decreases in activation (1, 2, 6). However, what remains unknown is the crucial issue of how the operation of these networks, identified in the resting state, relate to their function during cognitive information processing. Furthermore, the cognitive control mechanisms that mediate concurrent activation and deactiva...

Altered intrinsic organisation of brain networks implicated in attentional processes in adult attention-deficit/hyperactivity disorder: a resting-state study of attention, default mode and salience network connectivity

“…However, more recent models have introduced the crucial role of the SN to control the state-dependent switching between DMN and task-related attention networks [15]. Specifically, studies found support for a central role of the SN in attenuating the DMN and upregulating attention networks when switching from rest-to-task [19,20]. Interestingly, our results imply an intact between DMN and SN connectivity in ADHD, and indicate another locus of functional disorganisation that may relate to attention deficits, namely, the imbalance between SN and attention networks.…”

“…Support for this view comes from a range of recent studies [16][17][18][19][20]. 4 Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental condition characterised in part by symptoms of distractibility and an inability to ignore irrelevant stimuli -characteristics related to deficits in attentional control [21].…”

Processing social aspects of human gaze: A combined fMRI-DTI study

“…They found that gaze shifts increased the connectivity of right pSTS with the dorsal attention network including the right intraparietal sulcus (IPS) and right frontal eye field (FEF). The dorsal attention network is thought to control endogenous attention mechanisms to enhance sensory processing of task-relevant stimuli, whereas a more ventral attention system within the fronto-insular cortex comprising the anterior insula (aIns) and neighboring inferior frontal gyrus (IFG) may act as circuit-breaker that switch processing resources from the default mode network to the central-executive (Sridharan et al, 2008) and reorient attention toward unexpected but behaviorally significant stimuli (Corbetta et al, 2008).…”

Aging and large-scale functional networks: White matter integrity, gray matter volume, and functional connectivity in the resting state

“…The DMN was initially considered to represent neural baseline activity until further investigations showed that activity within the DMN is functionally related to internally driven mental states, such as self-referential processing, long-term memory, and mentalizing, and that its deactivation plays a functional role during externally directed tasks (Anticevic et al, 2012;Buckner et al, 2008;Burianova, McIntosh, & Grady, 2010;Kelly et al, 2008;Mennes et al, 2010;Sambataro et al, 2010). In addition, an emerging view suggests that cognitive performance in general might rely on the dynamic interaction between the DMN and two other large-scale neural networks: the fronto-parietal task-positive network (FPN), which is associated with attention and cognitive control, and the salience network (SN) in anterior cingulate and fronto-insular cortex, which is involved in the selection of emotionally and motivationally relevant stimuli (Andrews-Hanna et al, 2014;Chen et al, 2013;Fox et al, 2005;Seeley et al, 2007;Sridharan et al, 2008;Spreng et al, 2013). These three neural networks are central to cognition, as they are engaged in a large number of functions, and their disruption has been associated with a variety of clinical syndromes, such as schizophrenia, traumatic brain injury, and Alzheimer's disease (Manoliu et al, 2014;Sharp et al, 2014;Zhou et al, 2010).…”