Research ReportFronto-parietal networks underlie the interaction between executive control and conscious perception: Evidence from TMS and DWI
Introduction
Steadily a big amount of information is reaching our senses, creating a complex, changing, and highly-demanding environment. However, our processing capacities to deal with it are limited. It has been proposed that consciousness may have a role in reducing the noise and increasing the integration of information (Delacour, 1995). Attention is also known to play a key role in the selection of information, especially in crowded environments (Dehaene & Changeux, 2011; Posner, 1994). Following Posner and Petersen's taxonomy of attention (Petersen & Posner, 2012; Posner & Petersen, 1990), the executive control network is one of the three main attentional networks, together with the alerting and orienting networks. Executive control is implemented when situations involve novelty, planning, conflict detection/resolution, and error detection/correction (Norman & Shallice, 1986).
Many authors believe that attention and consciousness are closely related processes, although the nature of such relation is still under debate (Cohen & Dennett, 2011; Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006; Tallon-Baudry, 2012). At the behavioral level, different forms of attention have shown to interact with conscious perception (Chica, Lasaponara, Lupiáñez, Doricchi, & Bartolomeo, 2010; Kusnir, Chica, Mitsumasu, & Bartolomeo, 2011; Petersen, Petersen, Bundesen, Vangkilde, & Habekost, 2017). In particular, executive control modulates conscious perception (Martín-Signes, Paz-Alonso, & Chica, 2018), most likely influencing decision stages of processing (Colás, Capilla, & Chica, 2018; Colás, Triviño, & Chica, 2017). Exploring the neural mechanisms involved in attention and consciousness might provide clues on the nature of their relation. Namely, if attention and consciousness are related processes, shared or partially shared neural correlates are expected (Tallon-Baudry, 2012).
The frontal cortex (together with parietal regions) is crucial for cognitive control (Cocchi, Zalesky, Fornito, & Mattingley, 2013; Cole & Schneider, 2007; Diamond, 2013; Macdonald, Cohen, Stenger, & Carter, 2000) and, according with some theories, also for conscious perception. The global workspace theory (GWT) postulates that distributed large-scale brain networks linking higher visual areas to frontal and parietal cortex are essential for conscious perception (Dehaene et al., 2006; Dehaene, Kerszberg, & Changeux, 1998; Dehaene & Naccache, 2001; Del Cul, Dehaene, Reyes, Bravo, & Slachevsky, 2009; Rees, Kreiman, & Koch, 2002). However, the implication of frontal regions (and the fronto-parietal network) in conscious perception is in the center of a current debate (Boly et al., 2017; Bor & Seth, 2012; Odegaard, Knight, & Lau, 2017), with some authors arguing that frontal regions are only involved in the processes that emerge after conscious access (e.g., the reporting of the perceptual content or its cognitive manipulation; Tallon-Baudry, 2012).
If both systems (i.e. executive control and conscious perception) share neural resources, an interaction between both processes would be expected in frontal regions. A recent study (Martín-Signes et al., 2018) demonstrated an interaction between executive control and consciousness in the functional connectivity between a set of fronto-parietal regions (including left inferior frontal gyrus –IFG, left anterior cingulate cortex –ACC, left Frontal Eye Field –FEF, left inferior parietal lobe –IPL, right Supplementary Motor Area –SMA, and right superior parietal lobe –SPL). In this functional magnetic resonance imaging (fMRI) study, participants resolved a Stroop task presented at fixation while trying to detect near-threshold Gabor patches presented in the periphery. fMRI data demonstrated that functional connectivity increased between the left IFG-ACC, the left FEF-IPL, and the right SMA-SPL, for congruent trials when near-threshold Gabors were reported as compared to non-reported Gabors. No differences in functional connectivity between these regions were observed on incongruent trials.
According to theories such as the GWT, not only functional connectivity is important for conscious perception. Structural connectivity within the fronto-parietal network may be also key for conscious access. The Superior Longitudinal Fasciculus (SLF) is an extensive longitudinal white matter tract connecting the frontal and parietal lobes. It has been divided in three different branches: SLF I, SLF II and SLF III, labeled from dorsal to ventral. The SLF I extends between the superior parietal lobe and the dorsal and medial parts of the frontal lobe; the SLF II connects the angular gyrus and the posterior regions of the superior and middle frontal gyrus; the SLF III extends between the supramarginal gyrus and the inferior frontal gyrus (Nakajima, Kinoshita, Shinohara, & Nakada, 2019; Rojkova et al., 2016; Thiebaut de Schotten et al., 2011). The SLF has been linked to different attentional functions, including spatial orienting, sustained attention, and executive control in the healthy population (Sasson, Doniger, Pasternak, Tarrasch, & Assaf, 2012, 2013; Carretié, Ríos, Periáñez, Kessel, & Álvarez-Linera, 2012; Klarborg et al., 2013; Thiebaut de Schotten et al., 2011) and in different neurological conditions related with attention or awareness deficits (for example, spatial neglect, Doricchi, Thiebaut de Schotten, Tomaiuolo, & Bartolomeo, 2008; Thiebaut De Schotten et al., 2014; and attention-deficit/hyperactivity disorder, Chiang, Chen, Lo, Tseng, & Gau, 2015; Chiang, Chen, Shang, Tseng, & Gau, 2016; Wolfers et al., 2015). Newly, the microstructure of the right SLF III has been associated with the perceptual contrast needed to perceive near-threshold targets in patients with prefrontal damage (Colás et al., 2019). The neural interaction between conscious perception and different attentional subsystems has also been related to the microstructure of the SLF (Chica, Thiebaut de Schotten, Bartolomeo, & Paz-Alonso, 2018; Martín-Signes et al., 2018; Martín-Signes, Pérez-Serrano, & Chica, 2017).
The aim of this study was to explore the causal role of a frontal region in the interaction between executive control and conscious perception by using transcranial magnetic stimulation (TMS). To this aim, participants performed a Stroop task (to manipulate executive control, Stroop, 1935) concurrent with a detection task of near-threshold Gabor stimuli (see Colás et al., 2017). Based on previous correlational fMRI findings (Martín-Signes et al., 2018), the right SMA was selected as a target region (Experiment 1) because its functional connectivity with the right SPL demonstrated an interaction between executive control and conscious perception. The SMA has been traditionally linked to the motor control domain (Brass, 2002; Luppino, Matelli, Camarda, & Rizzolatti, 1993), however, especially the anterior part, is also linked to cognitive control functions (Miller & Cohen, 2001; Nachev, Kennard, & Husain, 2008). The right FEF was selected as an active control region (Experiment 2), because this region was related to conscious perception but not to the interaction between executive control and conscious perception. Based on previous observations demonstrating the role of the SLF in conscious perception, executive control, and the interaction between both processes (and its implication in other attentional systems), we also explored the role of the three branches of the SLF in the TMS effects over the expected behavioral interaction (as done before, Martín-Signes et al., 2017).
If our results show a causal role of the right SMA in the interaction between executive control and consciousness, this would add evidence in favor of shared neural correlates for executive control and conscious perception (Tallon-Baudry, 2012). The implication of a frontal region (i.e. the SMA) and its relation with the microstructural properties of SLF (a fronto-parietal tract) would constitute new evidence for the involvement of the fronto-parietal network in conscious perception.
Section snippets
Participants
G∗power (Faul, Erdfelder, Lang, & Buchner, 2007) was used to calculate sample size based on the effect size of a previously observed interaction between alerting and TMS region in a similar experiment (Martín-Signes et al., 2017; η2p = .38). We calculated sample size for a F test (interaction between Congruency and TMS region, α = .05; Power = .95). A sample of 24 participants was required. Therefore, 24 right-handed volunteers (12 females, mean age 24 years, standard deviation [SD] = 3.60)
Participants
24 right-handed volunteers (12 females, mean age 23 years, SD = 2.87) took part in the study.
Apparatus and stimuli, procedure and analysis
These were identical to Experiment 1 with the exception of the TMS target (Fig. 1B). The TMS stimulation sites were the right FEF (MNI coordinates: x = 36, y = −1, z = 53), which was extracted from a previous fMRI study (Martín-Signes et al., 2018), and the vertex. The mean TMS intensity applied was 60% of MSO (SD = 6.95). The mean right MT was 66% of the MSO. Stroop RTs shorter than 350 ms accounted
Discussion
The aim of this work was to explore the involvement of a frontal region, the right SMA, in the interaction between executive control and conscious perception by using TMS, a methodology that allows establishing causal relations by temporally modulating the state of the brain. In a dual task, executive control was manipulated with a Stroop task in which congruent and incongruent trials were presented at the same time that a near-threshold Gabor stimulus had to be detected. This work aims to
Authorship statement
Mar Martín-Signes: Methodology, Investigation, Formal analysis, Writing - Original Draft. Cristina Cano-Melle: Investigation. Ana B. Chica: Conceptualization, Methodology, Formal analysis, Writing - Review & Editing, Supervision, Funding acquisition.
Open practices
The study in this article earned an Open Materials badge for transparent practices. Materials and data for the study are available at https://osf.io/g8ue5/?view_only=b54ba6ec57b54810b92a220f402da6e8. The conditions of our ethics approval do not permit public archiving or sharing of anonymized raw study data. We report sample size calculations, all data exclusions, all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations,
Declaration of competing interest
None.
Acknowledgments
This work was supported by the Spanish Ministry of Economy and Competitiveness (MINECO; PSI2014-58681-P and PSI2017-88136-P grants to A.B.C.). M. M.-S. is supported by a predoctoral grant from the Spanish Ministry of Education, Culture and Sport (FPU15/04181). We thank Cristina Narganes-Pineda for providing health coverage during TMS sessions.
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2022, CortexCitation Excerpt :The SLF I is implicated in attention functions including top-down attention by connecting major frontoparietal network regions (Corbetta, Patel, & Shulman, 2008; Luna, Lupiáñez, & Martín-Arévalo, 2021). SLF III (particularly the right side) links attention and conscious perception and may identify salient events to facilitate attention maintenance (Chica, de Schotten, Bartolomeo, & Paz-Alonso, 2018; Martín-Signes, Cano-Melle, & Chica, 2021). Finally, the SLF II communicates between the SLF I and III, and may serve to direct attention based on salience information from SLF III (De Schotten et al., 2011; Nakajima, Kinoshita, Shinohara, & Nakada, 2020).
Differential involvement of frontoparietal network and insula cortex in emotion regulation
2021, NeuropsychologiaCitation Excerpt :Based on this framework, a variety of representative strategies can be applied to the three proposed ER processes (PVA) as follows: Attention allocation strategies (e.g., distraction) can be used to prevent the perception of an emotion, while cognitive change strategies (e.g., reappraisal) can be used to value emotion, and response modulation strategies (e.g., suppression) used to act on the emotion (Etkin et al., 2015; Morawetz et al., 2017b). The frontoparietal cortex, which is critical for cognitive control (Cocchi et al., 2013; Cole and Schneider, 2007; Martín-Signes et al., 2021), is activated during the aforementioned regulation strategies (Buhle et al., 2014; Morawetz et al., 2017b), and thus usually regarded as important cortical region of emotion control. In particular, the prefrontal cortex (PFC) plays a significant role in both generation and regulation of emotion (Dixon et al., 2017).