Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network Using Functional Magnetic Resonance Imaging

“Cerebral Cortex May 2011;21:1155--1165 doi:10.1093/cercor/bhq187 Advance Access publication October 5, 2010 Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network”

“Cerebral Cortex May 2011;21:1155--1165 doi:10.1093/cercor/bhq187 Advance Access publication October 5, 2010 Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network”

“Cerebral Cortex May 2011;21:1155--1165 doi:10.1093/cercor/bhq187 Advance Access publication October 5, 2010 Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network”

“Cerebral Cortex May 2011;21:1155--1165 doi:10.1093/cercor/bhq187 Advance Access publication October 5, 2010 Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network”

“In another study, Hampshire et al. (2010) compared different versions of a stop-signal task and found that the right IFC was activated regardless of the specific output required— response inhibition, response initiation, or internal counting— but that activation was greater in blocks requiring a…”

“…frontal cortex (IFC) in the inhibition of motor responses (Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et al. 2007; Leung and Cai 2007), suggesting…”

“…attentional reorienting and shifting (Corbetta and Shulman 2002; Hampshire and Owen 2006), oddball and target detection (McCarthy et al. 1997; Downar et al. 2000; Bledowski et al. 2004; Hampshire et al. 2007) and updating attended information (Hon et al. 2006), and is often coactivated with…”

“…involvement of the right inferior frontal cortex (IFC) in the inhibition of motor responses (Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et…”

“…studies of attention shifting identified, among other regions, an area in the left anterior intraparietal sulcus that showed consistent activation during different types of attentional shift (Wager et al. 2004) with a peak very close to the inferior parietal region identified in the present study.”

“…(Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et al. 2007; Leung and Cai 2007), suggesting that this region plays a specialized role in response inhibition.”

“…on shift trials and not stop trials, and therefore, this perceptual difference could lead to a difference in activation, these kinds of low-level perceptual differences are known to primarily evoke bilateral activation in color-sensitive visual cortical regions, such as V4 (Chawla et al. 1999).”

“In one study, Sharp et al. (2010) found that the right IFC/insula did not differentiate between 2 types of trials, both of which required the detection of a novel cue but only one of which required inhibition, suggesting that the detection of the novel cue was sufficient to activate this region.”

“In another study, Duann et al. (2009) examined the functional connectivity of different regions during motor inhibition and found that the pre-SMA but not the right IFC was directly connected to the basal ganglia, supporting differential roles for these regions in inhibitory control, with the right…”

“…of task demands, including attentional reorienting and shifting (Corbetta and Shulman 2002; Hampshire and Owen 2006), oddball and target detection (McCarthy et al. 1997; Downar et al. 2000; Bledowski et al. 2004; Hampshire et al. 2007) and updating attended information (Hon et al. 2006), and is…”

“Cerebral Cortex May 2011;21:1155--1165 doi:10.1093/cercor/bhq187 Advance Access publication October 5, 2010 Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network”

“An alternative hypothesis suggests that the IFC represents newly attended, task-relevant information as part of a ‘‘multiple demand’’ frontoparietal network recruited across a wide variety of different tasks (Duncan and Owen 2000; Duncan 2006).”

“…and shifting (Corbetta and Shulman 2002; Hampshire and Owen 2006), oddball and target detection (McCarthy et al. 1997; Downar et al. 2000; Bledowski et al. 2004; Hampshire et al. 2007) and updating attended information (Hon et al. 2006), and is often coactivated with the parietal cortex…”

“parietal regions and lower level sensory-specific cortex (Gazzaley et al. 2007; Browning et al. 2009; Lauritzen et al. 2009).”

“For example, Chikazoe et al. (2009) found that the right IFC showed significantly greater activation during inhibition trials, which required inhibition of a motor response, relative to ‘‘continue’’ trials, which did not require any change to the ongoing response.”

“with the strong connections of the right IFC with posterior brain regions (Pandya et al. 1996; Petrides and Pandya 1984), we would also argue that this interpretation rather neglects the”

“…studies have consistently demonstrated involvement of the right inferior frontal cortex (IFC) in the inhibition of motor responses (Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and…”

“…of motor responses (Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et al. 2007; Leung and Cai 2007), suggesting that this region plays a specialized…”

“…(Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et al. 2007; Leung and Cai 2007), suggesting that this region plays a specialized role in response inhibition.”

“parietal regions and lower level sensory-specific cortex (Gazzaley et al. 2007; Browning et al. 2009; Lauritzen et al. 2009).”

“…(Kawashima et al. 1996; Garavan et al. 1999; Konishi et al. 1999; Menon et al. 2001; Rubia et al. 2001; Aron et al. 2003; Kelly et al. 2004; Aron and Poldrack 2006; Li et al. 2006; Hodgson et al. 2007; Leung and Cai 2007), suggesting that this region plays a specialized role in response inhibition.”

“2007) and updating attended information (Hon et al. 2006), and is often coactivated with the parietal cortex in neuroimaging studies of executive function.”

“…(Corbetta and Shulman 2002; Hampshire and Owen 2006), oddball and target detection (McCarthy et al. 1997; Downar et al. 2000; Bledowski et al. 2004; Hampshire et al. 2007) and updating attended information (Hon et al. 2006), and is often coactivated with the parietal cortex in neuroimaging studies…”

“The concept of diversity as well as unity of PFC functions can be illustrated in a typical fMRI study [144] which had defined task components of response inhibition and cognitive flexibility, finding increased BOLD activity in the FPN including both the RIFG region and in the parietal cortex.”

“…for functional dissociations within the RIFG region that correspond to attentional and response inhibitory zones, and Dodds et al. have explicitly contrasted attentional and response control functions associated with the posterior parietal cortex and RIFG, respectively (Dodds et al., 2010).”

“…a more important role for the inferior frontal cluster in response inhibition than in monitoring outcomes of the task but does not exclude the possibility that this structure has other functions such as executive attention or overall motor control 78 and operates as a node in other neural networks.”

“The right IFG, besides detecting changes in stimulus features (Sharp et al. 2010; Dodds et al. 2010), facilitates infrequent action-related events by activating nondominant but relevant responses while inhibiting automatic but irrelevant actions at the same time.”

“…studies have shown increases in the activity of many regions within dAI network (dACC, MFG, SMG, FPA) during tasks that require attention/executive function (Barch et al., 1997; Cole and Schneider, 2007; Corbetta and Shulman, 2002; Dodds et al., 2011; Eichele et al., 2008; Kaller et al., 2011).”

“Yet, it might also be involved in attentional processing of a stop-signal (Boehler et al., 2011; Dodds et al., 2011; Hampshire et al., 2010; Sharp et al., 2010).”

“More broadly, our conclusions are also in line with those drawn on the basis of comparisons of the same Double Go task we used above [11] and alternative context monitoring tasks [8–10,23–24] with the Stop Signal task, as described below.”

“Our fi nding of increased activation in the rIFG combined with greater activation in other parts of the frontoparietal network is also compatible with the idea that the rIFG is not an isolated module, but plays a role in this larger network (cf., Dodds et al., 2011).”

“response inhibition and attentional control (e.g. Aron et al., 2004; Dodds et al., 2011; Hampshire et al., 2010) and the anterior insula with heightened awareness and emotional processing (e.”

“The core neural systems involved in response inhibition include inferior frontal gyrus, anterior insula cortex and dorsomedial frontal cortex (particularly the pre-supplementary motor area) (e.g. Aron, 2011; Aron et al., 2014; Cai and Leung, 2011; Chikazoe et al., 2009; Dodds et al., 2011; Meffert et al., 2015).”

“Previous neuroimaging study has demonstrated that right IFG involves in dissociating inhibition, attention, and response control in the frontoparietal network (115).”

“2009) and the integration of bottom-up sensory information with top-down response-related information (Dodds et al. 2011).”

“…postulated to be critical for supporting response inhibition (e.g. Aron et al., 2004; Aron, 2007), but recent theoretical and empirical work has argued that it is instead involved in contextual monitoring (Chatham et al., 2011; Dodds et al., 2011; Hampshire et al., 2010; Munakata et al., 2011).”

“The FPN includes primarily portions of the frontal cortex and parietal cortex, in which the lateral PFC is a core region (Vincent et al., 2008; Dodds et al., 2011; Cole et al., 2013; Smith et al., 2013).”

“, 2010) and greater response control (Dodds et al., 2011).”

“The role of the right inferior frontal gyrus (RIFG), associated with impulsive behaviour in healthy subjects and ADHD [38] is controversial [39,40].”

“Higher AINS activity is seen with increasing response control requirements (Dodds et al., 2011; Wu et al., 2019) and hard versus easy attentional demands (Deary et al., 2004; Brooks et al., 2017), while insula lesion reduces cognitive function under high load (Wu et al., 2019).”

“Another possible account for the increased RH involvement with increasing processing demands is that it reflects a greater need for more general cognitive processes, such as response selection and/or inhibition (e.g., Dodds et al., 2010).”

“Some studies suggest that the left PC but not the right PC is relevant to attentional shifting between taskrelevant stimuli (Dodds et al., 2011) and mediates the allocation of attentional resources toward the task-relevant stream such that the processing of the information is up-regulated (Liu et…”

“Recent works (Dodds et al., 2011) have found evidence that the right insula may be activated by a combination of attentional and response control demands, playing a role in the processing of sensory stimuli that are relevant to the current goals.”

“Furthermore, this argument is consistent with a recent study reporting a graded IFC response with increasing response control demands being associated with an increase in IFC activation (Dodds et al., 2011).”

“, 2014), especially when task requirements include switching (Dodds et al., 2011) and novelty aspects (Corbetta and Shulman, 2002).”

“, 2010). For example, Cai et al. (2011) directly measured corticomotor excitability on go trials in a stop context (cue signaling ‘maybe stop left/right’) by means of motor evoked potentials.”

“When making a decision, the association between the right insula and the inferior frontal cortex plays a crucial role in the integration of bottom-up, sensory information with top-down, response-related information to goal-directed behavior (Dodds et al., 2010).”

“More broadly, a similar area has often been reported in task manipulations that involve no obvious reward component at all— for example, response inhibition in the stop signal task (Aron et al., 2004; Dodds et al., 2011; Hampshire et al., 2010; Rubia et al., 2003), simple target detection (Hampshire et al.”

“…parietal lobule, bilateral insula and the midline cingulate and pre-SMA as canonical nodes of the RIC (Chen et al., 2009; Chevrier et al., 2007; Dodds et al., 2011; Fassbender et al., 2009, 2004; Garavan et al., 2006, 2008, 1999; Hampshire et al., 2010; Hester and Garavan, 2004; Kaufman et…”

“Studies on depression have increasingly focused on IFNs centered on the anterior cingulate cortex (ACC), a structure situated medially in the cerebral cortex and superior to the corpus callosum.”

“Previously, greater activation associated with shifting compared with stopping was reported in the left inferior parietal cortex [Dodds et al., 2011] though not in posterior medial areas.”

“Recent studies (Dodds et al., 2011) have found evidence that the right insula may be activated by a combination of attentional and response control demands, playing a role in the processing of sensory stimuli that are relevant to current goals.”

“…cannot conclude unequivocally that the hypoactivation resulted from inhibitory impairments per se rather than related executive functions such as performance monitoring (Li et al, 2006), specific task characteristics (Aichert et al, 2012), or increased response control demands (Dodds et al, 2011).”

“attentional functions in addition to response inhibition (Dodds et al., 2011; Hampshire et al., 2010, 2009).”

“The right inferior frontal gyrus and its associated networks may also have an important role in top-down response control, given that malfunction of this area is associated with impulsive behaviors.(14,15) Thus, distinct but inter-related neurocircuits may be relevant to the many facets of impulsivity.”

“First, although the dlPFC is a significant part of the frontoparietal control network, a flexible and superordinate system supporting adaptive behavioral control, 57,68 different brain regions of the frontoparietal network have shared and unique functions across a broad range of cognitive demands.”

“By contrast, a deficit in decision-making may be the result of impairments of cognitive brain functions, including cognitive control (Waskom et al 2016), monitor of action (Amodio and Frith 2006), attention (Dodds et al 2010) and goal maintenance (Sanfey et al 2003).”

“, 2010), although it may be the case that in order to evoke right IFG activity, the salience of these events must be relevant to response control (Dodds et al., 2011).”

“A specific role for right VLPFC in response inhibition, however, is a matter of significant debate (Dodds et al., 2010; Hampshire et al., 2010; Sharp et al., 2010).”

“Collectively, RIFG and insular cortex are thought to integrate sensory and cognitive information to facilitate goal-directed responses to stimuli in the environment (Dodds et al., 2011).”

“In healthy adults, this combined task has previously revealed stopping specific activation in the right inferior frontal cortex (IFC) and shifting specific activation in the left inferior parietal cortex (IPC), against a background of extensive co-activation for both in fronto-parietal regions (Dodds et al. 2011).”

“However, its involvement in successful response inhibition has been linked to other functions including attentional monitoring and the detection and processing of salient cues [Chao et al., 2009; Dodds et al., 2011; Duann et al., 2009; Hampshire et al., 2010; Hester et al., 2004; Li et al., 2006; Sharp et al., 2010].”

“Moreover, it has recently been suggested in the context of a modified Go-NoGo task that the requirements for response control irrespective of response inhibition can also strongly activate the right IFG [29].”

“The right IFG has been previously associated with switching to alternative responses and withholding responses (Kenner et al, 2010; Dodds et al, 2011).”

“integrates inhibitory and attentional control to produce flexible, goal-directed behavior (Dodds et al., 2011).”

“Many previous fMRI studies focused on dissociations between executive functions, suggesting they are supported by functionally distinct territories of the association cortices (Wager et al. 2005; Dosenbach et al. 2006; Dodds et al. 2011; Hampshire et al. 2012; Eisenreich et al. 2017).”

“The right lateral IFG is involved in both attentional and response control (Dodds et al., 2011; Hampshire et al., 2010) and has been referred to as a “brake”, because it is important for pausing and braking responses, in addition to outright stopping (Aron et al., 2014).”

“However, note that our results also fit with findings and claims of other authors proposing that rIFG, rTPG, and rMFG activity may not be specific for one mental process, but rather reflect an interplay of multiple processes in complex cognitive tasks [Corbetta et al., 2008; Corbetta and Shulman, 2002; Dodds et al., 2…”

“Recent fMRI studies [34,35,36,37,38,39] have helped delineate distinct roles for the IFG and pre-SMA in SST and Go/No-Go task performance: The IFG is activated during the control of motor responses and successful stopping, but also more generically in response to presentations of infrequent visually-salient stimuli, a…”

“…parietal lobule, bilateral insula and the midline cingulate and pre-SMA as canonical nodes of the RIC (Chen et al., 2009; Chevrier et al., 2007; Dodds et al., 2011; Fassbender et al., 2009, 2004; Garavan et al., 2006, 2008, 1999; Hampshire et al., 2010; Hester and Garavan, 2004; Kaufman et…”