Basic research The frontoparietal network: function, electrophysiology, and importance of individual precision mapping Scott Marek, PhD; Nico U. F. Dosenbach, MD, PhD Introduction he human brain is unique among other species in its abilityT to accurately and rapidly learn new concepts and switch between states, while maintaining complex rule sets. We engage in countless goal-directed tasks throughout a given day, adopting task sets that flexibly The frontoparietal network is critical for our ability to configure information processing in response to chang- coordinate behavior in a rapid, accurate, and flexible ing task demands. In cognitive psychology and neuro- goal-driven manner. In this review, we outline support science, this process of volitional goal-driven behavior for the framing of the frontoparietal network as a dis- is referred to as cognitive control. Cognitive control is tinct control network, in part functioning to flexibly in- not executed by a single brain region or single brain teract with and alter other functional brain networks. network, but rather by several largely non-overlapping This network coordination likely occurs in a 4 Hz to13 brain networks, each consisting of a relatively large set Hz θ/α rhythm, both during resting state and task state. of anatomically distributed regions, including the fron- Precision mapping of individual human brains has re- toparietal, cingulo-opercular, and salience networks. vealed that the functional topography of the frontopa- There is now abundant evidence that these networks rietal network is variable between individuals, under- are anatomically separate from downstream process- scoring the notion that group-average studies of the ing or attention networks, both during task states and frontoparietal network may be obscuring important typical and atypical features. Many forms of psychopa- Keywords: cognitive control; cognitive flexibility; frontoparietal; lateral prefrontal cortex; intraparietal sulcus; psychopathology thology implicate the frontoparietal network, such as schizophrenia and attention-deficit/hyperactivity dis- Author affiliations: Department of Neurology, Washington University School of Medicine, St Louis, Missouri, USA (Scott Marek, Nico U. F. Dosen- order. Given the interindividual variability in frontopa- bach); Program in Occupational Therapy, Washington University School of rietal network organization, clinical studies will likely Medicine, St Louis, Missouri, USA (Nico U. F. Dosenbach); Department of benefit greatly from acquiring more individual subject Pediatrics, Washington University School of Medicine, St Louis, Missouri, USA (Nico U. F. Dosenbach) data to accurately characterize resting-state networks compromised in psychopathology. Address for correspondence: Scott Marek, Postdoctoral Research Scholar, Washington University in St. Louis, Department of Neurology, St. Louis, © 2018, AICH – Servier Group Dialogues Clin Neurosci. 2018;20:133-140. MO 63110, USA (email: [email protected]) Copyright © 2018 AICH – Servier Group. All rights reserved 133 www.dialogues-cns.org Basic research the resting state. Each network plays a unique role in prefrontal cortex, which in turn exert top-down control. cognitive control, including its implementation, main- Since this time, the conflict monitoring hypothesis has tenance, and updating. Networks related to attention vs evolved, prescribing a role of dorsal anterior cingulate cognitive control map onto those outlined by Petersen in signaling the expected value of control.8 Working and Posner,1,2 with the dorsal and ventral attention net- closely in conjunction with this region and comprising works supporting orienting and the frontoparietal and the core of the brain’s salience network, the anterior cingulo-opercular networks supporting cognitive con- insula is thought to detect salient features for additional trol. For the duration of this review, we will be focused processing and is thought to act as a switchboard to di- on the control networks, with emphasis on the fronto- rect other brain networks.9-11 parietal control network. Although the conflict-monitoring hypothesis as- We begin our review by summarizing evidence for cribes the anterior cingulate a central role in control, the frontoparietal network as distinct from other con- a separate dual network’s view holds that cognitive trol and attention networks, including its privileged role control is supported by multiple, anatomically distrib- as a flexible hub of cognitive control. We then move into uted brain networks.12 This model is the result of stud- a discussion of the oscillations underlying frontopari- ies specifically aiming to delineate distinct control sig- etal network interactions, during both resting and task nals. Though the detection of salient stimuli and conflict states. Following this, we will discuss the importance of resolution are essential features of cognitive control, densely sampling individual subjects. There is compel- humans also need to maintain and adapt control. Thus, ling evidence that while core regions of the frontopari- there are three main signals related to cognitive control: etal network are present across individuals, critical vari- (i) a transient signal resulting from the realization of the ants in this network’s topography exist. We conclude by need to instantiate control; (ii) a sustained signal sup- briefly reviewing evidence for frontoparietal dysfunc- porting the maintenance of control; and (iii) a transient tion in several forms of psychopathology that emerge signal supporting performance feedback. An early at- during adolescence, a time when the frontoparietal tempt to disentangle brain regions supporting different network is refining many of its interactions with other modes of control was executed by Braver and colleagues brain networks. Given the anatomical heterogeneity of using a mixed block/event related design in functional the frontoparietal network across individuals, we argue magnetic resonance imaging (fMRI).13 Results from a complimentary shift towards densely sampling indi- this study concluded that the anterior prefrontal cortex vidual subjects in both normative and diseased states is was most reliably activated during the maintenance of of paramount importance to understanding the fronto- control, while the superior parietal lobes were involved parietal network in typical and atypical cohorts. in transient control. Several years later, Dosenbach and colleagues executed a cross-studies analysis on 10 Evidence for parallel, segregated mixed block/event-related fMRI studies to tease apart control networks regions contributing to the main signals contributing to cognitive control.12 These tasks included visual and The original focus on the anatomical substrate of cog- auditory stimuli, with many different decision criteria, nitive control was within the anterior cingulate cortex such as semantic, timing, and similarity judgments. They and to a lesser extent the anterior insula. This is because discovered a set of regions including the anterior pre- the anterior cingulate demonstrates reliable activation frontal, anterior insular, and anterior cingulate cortices in response to many forms of control, including, but that showed preferable activation for the maintenance not limited to, task switching, novelty detection, focal of control, whereas the bilateral intraparietal sulcus and attention, and error commission.3-6 This early work led lateral prefrontal cortex showed preferable activation Botvinick and colleagues to conclude that the anterior for task-set initiation. Lastly, performance feedback cingulate facilitates outcome monitoring by evaluating seemed to be supported by the inferior parietal lobe, the result of an individual’s actions, and facilitating the dorsolateral prefrontal cortex, and lateral cerebellum.12 resolution of conflict during task (ie, conflict monitor- During the mid-2000s, fMRI analysis was shifting ing).7 Thus, it was proposed that the anterior cingulate from a focus on regional contributions to brain func- acts to alert regulatory regions, such as the dorsolateral tion to a broader network-level focus. With respect to 134 Frontoparietal control network - Marek and Dosenbach Dialogues in Clinical Neuroscience - Vol 20 . No. 2 . 2018 this network-level approach, a key observation is that lated α-band activity in downstream visual association co-fluctuations during the resting-state largely recapit- cortices, whereas there was no evidence for top-down ulate patterns of activation during task.14 Capitalizing modulation of the visual network by the cingulo-oper- on this observation, Dosenbach and colleagues imple- cular network, supporting a role for the frontoparietal mented resting-state fMRI to delineate a whole brain network in bias sensory information in processing net- network’s view of the brain’s control architecture.15,16 works.20,21 During the resting state, two largely parallel control networks emerged. These two distinct networks were Role of the frontoparietal network: coined the frontoparietal and cingulo-opercular net- a flexible hub for cognitive control works. The original putative role of the cingulo-opercu- lar network was in the flexible control of goal-directed Humans are unique and quite remarkable in their de- behavior through the stable implementation of task gree of flexibility and speed when instantiating cogni- sets in downstream sensorimotor processors across tri- tive control. How the human brain is capable of doing als, while control