Flexible interactions between brain regions enable neural systems to adaptively transfer and process information. However, the neural substrates that regulate adaptive communications between brain regions are understudied. In this human fMRI study, we investigated this issue by tracking time-varying, task-evoked changes in functional connectivity between localized occipitotemporal regions while participants performed different tasks on the same visually presented stimuli. We found that functional connectivity between ventral temporal and the primary visual regions selectively increased during the processing of task-relevant information. Further, additional task demands selectively strengthen these targeted connectivity patterns. To identify candidate regions that contribute to this increase in inter-regional coupling, we regressed the task-specific time-varying connectivity strength between primary visual and occipitotemporal regions against voxel-wise activity patterns elsewhere in the brain. This allowed us to identify a set of frontal and parietal regions whose activity increased as a function of task-evoked functional connectivity. These results suggest that frontoparietal regions may provide top-down biasing signals to influence task-specific interactions between brain regions.

Hierarchical cognitive control enables us to execute actions guided by abstract goals. Previous research has suggested that neuronal oscillations at different frequency bands are associated with top-down cognitive control; however, whether distinct neural oscillations have similar or different functions for cognitive control is not well understood. The aim of the current study was to investigate the oscillatory neuronal mechanisms underlying two distinct components of hierarchical cognitive control: the level of abstraction of a rule, and the number of rules that must be maintained (set-size). We collected EEG data in 31 men and women who performed a hierarchical cognitive control task that varied in levels of abstraction and set-size. Results from time-frequency analysis in frontal electrodes showed an increase in theta amplitude for increased set-size, whereas an increase in δ was associated with increased abstraction. Both theta and δ amplitude correlated with behavioral performance in the tasks but in an opposite manner: theta correlated with response time slowing when the number of rules increased, whereas δ correlated with response time when rules became more abstract. Phase-amplitude coupling analysis revealed that δ phase-coupled with β amplitude during conditions with a higher level of abstraction, whereby beta band may potentially represent motor output that was guided by the δ phase. These results suggest that distinct neural oscillatory mechanisms underlie different components of hierarchical cognitive control.SIGNIFICANCE STATEMENT Cognitive control allows us to perform immediate actions while maintaining more abstract, overarching goals in mind and to choose between competing actions. We found distinct oscillatory signatures that correspond to two different components of hierarchical control: the level of abstraction of a rule and the number of rules in competition. An increase in the level of abstraction was associated with δ oscillations, whereas theta oscillations were observed when the number of rules increased. Oscillatory amplitude correlated with behavioral performance in the task. Finally, the expression of β amplitude was coordinated via the phase of δ oscillations, and theta phase-coupled with γ amplitude. These results suggest that distinct neural oscillatory mechanisms underlie different components of hierarchical cognitive control.

Beta and gamma frequency neuronal oscillations have been implicated in top-down and bottom-up attention. In this study, we used rhythmic TMS to modulate ongoing beta and gamma frequency neuronal oscillations in frontal and parietal cortex while human participants performed a visual search task that manipulates bottom-up and top-down attention (single feature and conjunction search). Both task conditions will engage bottom-up attention processes, although the conjunction search condition will require more top-down attention. Gamma frequency TMS to superior precentral sulcus (sPCS) slowed saccadic RTs during both task conditions and induced a response bias to the contralateral visual field. In contrary, beta frequency TMS to sPCS and intraparietal sulcus decreased search accuracy only during the conjunction search condition that engaged more top-down attention. Furthermore, beta frequency TMS increased trial errors specifically when the target was in the ipsilateral visual field for the conjunction search condition. These results indicate that beta frequency TMS to sPCS and intraparietal sulcus disrupted top-down attention, whereas gamma frequency TMS to sPCS disrupted bottom-up, stimulus-driven attention processes. These findings provide causal evidence suggesting that beta and gamma oscillations have distinct functional roles for cognition.

The thalamus is globally connected with distributed cortical regions, yet the functional significance of this extensive thalamocortical connectivity remains largely unknown. By performing graph-theoretic analyses on thalamocortical functional connectivity data collected from human participants, we found that most thalamic subdivisions display network properties that are capable of integrating multimodal information across diverse cortical functional networks. From a meta-analysis of a large dataset of functional brain-imaging experiments, we further found that the thalamus is involved in multiple cognitive functions. Finally, we found that focal thalamic lesions in humans have widespread distal effects, disrupting the modular organization of cortical functional networks. This converging evidence suggests that the human thalamus is a critical hub region that could integrate diverse information being processed throughout the cerebral cortex as well as maintain the modular structure of cortical functional networks.SIGNIFICANCE STATEMENT The thalamus is traditionally viewed as a passive relay station of information from sensory organs or subcortical structures to the cortex. However, the thalamus has extensive connections with the entire cerebral cortex, which can also serve to integrate information processing between cortical regions. In this study, we demonstrate that multiple thalamic subdivisions display network properties that are capable of integrating information across multiple functional brain networks. Moreover, the thalamus is engaged by tasks requiring multiple cognitive functions. These findings support the idea that the thalamus is involved in integrating information across cortical networks.

Past studies have demonstrated that flexible interactions between brain regions support a wide range of goal-directed behaviors. However, the neural mechanisms that underlie adaptive communication between brain regions are not well understood. In this study, we combined theta-burst transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging to investigate the sources of top-down biasing signals that influence task-evoked functional connectivity. Subjects viewed sequences of images of faces and buildings and were required to detect repetitions (2-back vs. 1-back) of the attended stimuli category (faces or buildings). We found that functional connectivity between ventral temporal cortex and the primary visual cortex (VC) increased during processing of task-relevant stimuli, especially during higher memory loads. Furthermore, the strength of functional connectivity was greater for correct trials. Increases in task-evoked functional connectivity strength were correlated with increases in activity in multiple frontal, parietal, and subcortical (caudate and thalamus) regions. Finally, we found that TMS to superior intraparietal sulcus (IPS), but not to primary somatosensory cortex, decreased task-specific modulation in connectivity patterns between the primary VC and the parahippocampal place area. These findings demonstrate that the human IPS is a source of top-down biasing signals that modulate task-evoked functional connectivity among task-relevant cortical regions.

INTRODUCTION: Top-down control underlies our ability to attend relevant stimuli while ignoring irrelevant, distracting stimuli and is a critical process for prioritizing information in working memory (WM). Prior work has demonstrated that top-down biasing signals modulate sensory-selective cortical areas during WM, and that the large-scale organization of the brain reconfigures due to WM demands alone; however, it is not yet understood how brain networks reconfigure between the processing of relevant versus irrelevant information in the service of WM. METHODS: Here, we investigated the effects of task goals on brain network organization while participants performed a WM task that required participants to detect repetitions (e.g., 0-back or 1-back) and had varying levels of visual interference (e.g., distracting, irrelevant stimuli). We quantified changes in network modularity-a measure of brain sub-network segregation-that occurred depending on overall WM task difficulty as well as trial-level task goals for each stimulus during the task conditions (e.g., relevant or irrelevant). RESULTS: First, we replicated prior work and found that whole-brain modularity was lower during the more demanding WM task conditions compared to a baseline condition. Further, during the WM conditions with varying task goals, brain modularity was selectively lower during goal-directed processing of task-relevant stimuli to be remembered for WM performance compared to processing of distracting, irrelevant stimuli. Follow-up analyses indicated that this effect of task goals was most pronounced in default mode and visual sub-networks. Finally, we examined the behavioral relevance of these changes in modularity and found that individuals with lower modularity for relevant trials had faster WM task performance. DISCUSSION: These results suggest that brain networks can dynamically reconfigure to adopt a more integrated organization with greater communication between sub-networks that supports the goal-directed processing of relevant information and guides WM.