Review
Oscillatory Dynamics of Prefrontal Cognitive Control

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Prefrontal oscillatory dynamics coordinate cortical and subcortical large-scale networks, providing a functional basis for flexible cognitive control of goal-directed behavior and do not constitute an epiphenomenon of spiking activity.

Nonlinear dynamics, including phase resetting, endogenous entrainment, and CFC, support the spatiotemporal organization of functional networks and predict behavior on the single-trial level.

Neuronal oscillations provide the temporal reference frame for activity-silent encoding in neuronal assemblies, which complements the view that the neuron is the structural and functional unit of the nervous system.

Multiplexing on different temporal channels reflects distinct canonical computations and increases cortical coding capacity.

Directionality analyses reveal the timing of information flow along established anatomical pathways.

The prefrontal cortex (PFC) provides the structural basis for numerous higher cognitive functions. However, it is still largely unknown which mechanisms provide the functional basis for flexible cognitive control of goal-directed behavior. Here, we review recent findings that suggest that the functional architecture of cognition is profoundly rhythmic and propose that the PFC serves as a conductor to orchestrate task-relevant large-scale networks. We highlight several studies that demonstrated that oscillatory dynamics, such as phase resetting, cross-frequency coupling (CFC), and entrainment, support PFC-dependent recruitment of task-relevant regions into coherent functional networks. Importantly, these findings support the notion that distinct spectral signatures reflect different cortical computations supporting effective multiplexing on different temporal channels along the same anatomical pathways.

Section snippets

The Functional Architecture of Cognition Is Rhythmic

Cognition and the executive control of goal-directed behavior are highly flexible and rapidly integrate task-relevant information according to the current contexts and demands. However, the neuronal basis of higher cognitive functions is still largely unknown. Results from numerous lesion studies have suggested that the PFC is essential for the organization and control of goal-directed behavior [1]. In addition, various reports have emphasized the role of PFC activity patterns, thought to

Oscillatory Mechanisms Guiding Behavior and Cognition

Classic models of cognitive processing, such as the drift diffusion model for decision-making or the persistent delay activity model of working memory (WM), emphasize the importance of the activation of single neurons for effective cortical processing [23]. These models have recently been questioned by several studies 24, 25, 26. For example, it has been suggested that sustained activity at the population level reflects an artifact of averaging across multiple trials with different onset

Prefrontal Cortex Dependent Large-Scale Networks

It has long been suspected that cognitive control and the means to achieve fluid goal-directed behavior stem from activity patterns in the PFC, which selectively bias neuronal activity in distant cortical and subcortical regions and control the information flow in large-scale neuronal networks [2]. The popular communication-through-coherence (CTC) hypothesis suggested that neuronal communication is established through coherently oscillating neuronal assemblies [4]. Over the past decade,

Multiplexed Cognition and its Spatiotemporal Organization

Results from several single-unit studies indicate that neuronal populations in the PFC exhibit a mixed selectivity 64, 65, 66, 67, 68; that is, these populations are able to engage in different tasks facilitating cognitive flexibility. However, it is unknown how these neuronal assemblies are recruited into an active circuit while simultaneously providing feedback to downstream regions. It has been suggested that temporal multiplexing constitutes a key mechanism of prefrontal integrative

Entrainment as a Mechanism of Top-Down Control

The directionality of complex neuronal interactions across several spatiotemporal scales is often difficult to infer, since oscillatory signals are periodic in nature, often lack a defined beginning, and may also be confounded by evoked activity. Several methods have been proposed to estimate directionality in electrophysiological recordings (Box 2). Currently, Granger causality (GC [79]) is among one of the most popular techniques. A recent study investigating PFC–striatum interactions during

Linking Structural and Functional Connectivity

Structural and functional connectivity and their relation to behavior are often studied in isolation. While structural connectivity is mainly assessed by diffusion imaging, functional connectivity can be inferred by circular or linear correlation analyses of band-limited electrophysiological signals (Figure 3A) [3]. Several studies have begun to unravel the structural and functional architecture of the frontoparietal network and its role for spatial attention 85, 86, 87. Decreased alpha and

Oscillopathies and Network Disorders

The synchronization of neuronal oscillations across several spatiotemporal scales constitutes a hallmark of the physiological brain function 3, 7, 18. Hence, numerous neuropsychiatric diseases have been associated with pathological changes in oscillatory processes. In particular, the symptoms of Parkinson's disease (PD) might be caused by abnormal oscillatory activity. For example, Parkinson rigidity has been linked to elevated CFC between the basal ganglia and motor cortex [94]. However, it is

Concluding Remarks

Neuronal oscillations have been considered an epiphenomenon in the past. However, over the past decade, several findings have demonstrated that oscillations guide cortical spiking activity [6] and have a causal role in conscious perception and cognitive processing 5, 18, 19, 104, 105, 106. In particular, several lines of research have provided evidence that cognition emerges from coordinated neuronal activity in specialized yet widely distributed cortical regions 3, 4, 81. Although lesion

Acknowledgments

This work was supported by a NINDS Javits Award R37NS21135 (R.T.K.), the Nielsen Corporation (R.T.K.), the German Research Foundation (DFG SFB936/A3/Z1), an intramural research grant from the Department of Psychology, University of Oslo, and the Alexander von Humboldt Foundation (Feodor Lynen Program, R.F.H.).

Glossary

Activity-silent encoding
traditionally, active processing has been associated with an increase in neuronal spiking or high frequency activity (HFA). However, meaningful processing with behavioral consequences has also been observed without changes in spiking and is referred to as ‘activity silent’.
Cognitive control
summarizes various executive functions, such as attention, working memory, error monitoring, inhibitory control, or planning, which reflect the means to achieve fluid behavior.

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