Significance: The brain is never at rest, and patterns of ongoing correlated activity have been found to resemble patterns during active behavior. A fundamental problem in neuroscience concerns the relationship between spontaneous and task-driven activity. During a demanding task that requires selective attention to sensory stimuli, correlated patterns of spontaneous (rest) activity are generally preserved. However, specific changes in synchronization occur within and between networks that correlate with behavioral performance. These results indicate that attention modifies spontaneous activity patterns in support of task performance.

We investigated the functional properties of a previously described cingulo-opercular network (CON) putatively involved in cognitive control. Analyses of common fMRI task-evoked activity during perceptual and episodic memory search tasks that differently recruited the dorsal attention (DAN) and default mode network (DMN) established the generality of this network. Regions within the CON (anterior insula/frontal operculum and anterior cingulate/presupplementary cortex) displayed sustained signals during extended periods in which participants searched for behaviorally relevant information in a dynamically changing environment or from episodic memory in the absence of sensory stimulation. The CON was activated during all phases of both tasks, which involved trial initiation, target detection, decision, and response, indicating its consistent involvement in a broad range of cognitive processes. Functional connectivity analyses showed that the CON flexibly linked with the DAN or DMN regions during perceptual or memory search, respectively. Aside from the CON, only a limited number of regions, including the lateral pFC, showed evidence of domain-general sustained activity, although in some cases the common activations may have reflected the functional-anatomical variability of domain-specific regions rather than a true domain generality. These additional regions also showed task-dependent functional connectivity with the DMN and DAN, suggesting that this feature is not a specific marker of cognitive control. Finally, multivariate clustering analyses separated the CON from other frontoparietal regions previously associated with cognitive control, indicating a unique fingerprint. We conclude that the CON's functional properties and interactions with other brain regions support a broad role in cognition, consistent with its characterization as a task control network.

Alpha (8–12 Hz) power desynchronization is strongly associated to visual perception but has been observed in a large variety of tasks, indicating a general role in task anticipation. We previously reported in human observers that interference by repetitive transcranial magnetic stimulation (rTMS) of core regions of the dorsal attention network (DAN) disrupts both anticipatory alpha desynchronization and performance during a visuospatial attention (VSA) task. Here, we test the hypothesis that alpha desynchronization is task specific, and can be selectively modulated by interfering with activity in different higher-order parietal regions. We contrast the effects of rTMS on alpha rhythms and behavior on 2 different tasks: a VSA and a semantic decision task, by targeting the posterior intraparietal sulcus (pIPS), a core region of the DAN, or the angular gyrus (AG), a core region of the default mode network (DMN). We found that both performance and anticipatory alpha desynchronization were affected by stimulation of IPS only during VSA, and of AG only during semantic decisions. These findings indicate the existence of multiple dedicated parietal channels for the modulation of anticipatory alpha rhythms, which in turn reflect task-specific modulation of excitability in human parieto-occipital cortex.

Visual selection requires mechanisms for representing object salience and for shifting the focus of processing to novel objects. It is not clear from computational or neural models whether these operations are performed within the same or different brain regions. Here, we use repetitive transcranial magnetic stimulation to briefly interfere with neural activity in individually localized regions of human posterior parietal cortex (PPC) that are putatively involved in attending to contralateral locations or shifting attention between locations. Stimulation over right ventral intraparietal sulcus impaired target discrimination at contralateral locations, whereas stimulation over right medial superior parietal lobule impaired target discrimination after a shift of attention regardless of its location. This double dissociation is consistent with neuroimaging studies and indicates that mechanisms of visual selection are partly anatomically segregated in human PPC.

Neuroimaging studies conducted in the last three decades have distinguished two frontoparietal networks responsible for the control of visuospatial attention. The present review summarizes recent findings on the neurophysiological mechanisms implemented in both networks and describes the evolution from a model centered on the distinction between top-down and bottom-up attention to a model that emphasizes the dynamic interplay between the two networks based on attentional demands. The role of the dorsal attention network (DAN) in attentional orienting, by boosting behavioral performance, has been investigated with multiple experimental approaches. This research effort allowed us to trace a distinction between DAN regions involved in shifting vs. maintenance of attention, gather evidence for the modulatory influence exerted by the DAN over sensory cortices, and identify the electrophysiological correlates of the orienting function. Simultaneously, other studies have contributed to reframing our understanding of the functions of the ventral attention network (VAN) and its relevance for behavior. The VAN is not simply involved in bottom-up attentional capture but interacts with the DAN during reorienting to behaviorally relevant targets, exhibiting a general resetting function. Further studies have confirmed the selective rightward asymmetry of the VAN, proposed a functional dissociation along the anteroposterior axis, and suggested hypotheses about its emergence during the evolution of the primate brain. Finally, novel models of network interactions explain the expression of complex attentional functions and the emergence and restorations of symptoms characterizing unilateral spatial neglect. These latter studies emphasize the importance of considering patterns of network interactions for understanding the consequences of brain lesions.

Using repetitive transcranial magnetic stimulation (rTMS), we have recently shown a functional anatomical distinction in human parietal cortex between regions involved in maintaining attention to a location [ventral intraparietal sulcus (vIPS)] and a region involved in shifting attention between locations [medial superior parietal lobule (mSPL)]. In particular, while rTMS interference over vIPS impaired target discrimination at contralateral attended locations, interference over mSPL affected performance following shifts of attention regardless of the visual field (Capotosto et al., 2013). Here, using rTMS interference in conjunction with EEG recordings of brain rhythms during the presentation of cues that indicate to either shift or maintain spatial attention, we tested whether this functional anatomical segregation involves different mechanisms of rhythm synchronization. The transient inactivation of vIPS reduced the amplitude of the expected parieto-occipital low-α (8–10 Hz) desynchronization contralateral to the cued location. Conversely, the transient inactivation of mSPL, compared with vIPS, reduced the high-α (10–12 Hz) desynchronization induced by shifting attention into both visual fields. Furthermore, rTMS induced a frequency-specific delay of task-related modulation of brain rhythms. Specifically, rTMS over vIPS or mSPL during maintenance (stay cues) or shifting (shift cues) of spatial attention, respectively, caused a delay of α parieto-occipital desynchronization. Moreover, rTMS over vIPS during stay cues caused a delay of δ (2–4 Hz) frontocentral synchronization. These findings further support the anatomo-functional subdivision of the dorsal attention network in subsystems devoted to shifting or maintaining covert visuospatial attention and indicate that these mechanisms operate in different frequency channels linking frontal to parieto-occipital visual regions.