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The Dorsal Frontoparietal Network: A Core System for Emulated Action

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Abundant functional imaging research supports a comprehensive role of the dFPN in multiple motor and cognitive functions.

These functions can be pinned down to a common ‘core’ computation whose essential role it is to establish abstract representations of movement kinematics: action emulation.

Through synergy and recombination of basic cognitive components, more complex functions emerge from action emulation during child development.

The dFPN eventually assumes a domain-general role in spatial attention and working memory, laying the foundation for general reasoning, decision making, and intelligence.

The dorsal frontoparietal network (dFPN) of the human brain assumes a puzzling variety of functions, including motor planning and imagery, mental rotation, spatial attention, and working memory. How can a single network engage in such a diversity of roles? We propose that cognitive computations relying on the dFPN can be pinned down to a core function underlying offline motor planning: action emulation. Emulation creates a dynamic representation of abstract movement kinematics, sustains the internal manipulation of this representation, and ensures its maintenance over short time periods. Based on these fundamental characteristics, the dFPN has evolved from a pure motor control network into a domain-general system supporting various cognitive and motor functions.

Section snippets

The Domain-General Role of Dorsal Frontoparietal Cortex

Human cognition is sustained by structurally and functionally organized networks of the brain, often labeled using broad anatomical or functional descriptors 1, 2, 3. One of the most prominent, the dFPN (see Glossary), connects the superior parietal cortex with dorsal premotor cortex (PMd) [4]. These regions exhibit a strongly correlated pattern of activation at rest and during various motor or cognitive tasks, such as reaching and grasping, saccades and spatial attention, mental rotation, or

An Outline of the Emulation Account of dFPN Function

Action emulation is the abstract, offline representation of movements expressed in terms of their pragmatics (action goals) and kinematics (movement patterns). The term ‘emulation’ is borrowed from computer science, where it describes the ability of a program to imitate the behavior of other programs. The existence of emulation processes in motor planning is inferred from the observation that motor control relies on predictions of the consequences of motor plans (Figure 1A). Performing a

The dFPN Is a Common Substrate for Motor and Cognitive Processes

One of the central tenets that the action emulation account has in common with other accounts is that a more complex cognitive process may emerge from simpler processes if it shares neural sources and uses overlapping computational mechanisms. Resting-state fMRI connectivity defines the anatomy of the dFPN (Box 1) and provides tentative support for this assumption. Although resting-state oscillations do not inform about the cognitive processes occurring in a network, they suggest that

Interdependencies between Motor and Cognitive Functions Sustained by the dFPN

The first prediction of the emulation account is that behavioral studies should support a common functional origin of real and simulated action. Given that simulated movement cannot be directly observed, much of the evidence favoring this point is deduced from reaction times for real and imagined actions [65]. For example, the duration of real movements and estimated durations of imagined movements are indistinguishable for horizontal, uphill or downhill walking [66], hand rotation [67], mental

Structural and Virtual Damage of the dFPN

The emulation account further predicts that action planning, mental rotation, spatial attention, and working memory should all suffer following damage to the dorsal premotor and parietal cortex. PPC lesions lead to severe deficits of goal-oriented movements, known as optic ataxia, which are particularly evident in peripheral vision and when online correction of movement is required 89, 90. Electrical stimulation of the PPC evokes an intention to move, or even the belief that the contralateral

Concluding Remarks

Domain-general cognitive systems are a distinctive feature of the human mind, forming the bedrock for the remarkable evolutionary expansion of reasoning capacity and general intelligence in humans. How domain-general properties are acquired has been a source of much theorizing. Functional imaging, behavioral, developmental, and human lesion studies support the hypothesis that the domain-general role of the dFPN evolved through synergy between isolated cognitive components and the core function

Acknowledgments

Supported by grants from the Swiss National Science Foundation and the Novartis Foundation. We wish to thank Britt Anderson, Klemens Gutbrod, Georg Kerkhoff, René Müri, and Guy Vingerhoets, as well as three anonymous reviewers, whose insightful comments contributed to shape our arguments.

Glossary

Dorsal frontoparietal network (dFPN)
functional network connecting the superior parietal cortex with the dorsal premotor cortex.
Efference copy
internal copy of a motor plan that becomes available to sensory and cognitive systems generating a prediction of movement outcome.
Emulation
abstract representation and offline maintenance of the kinematic properties of a movement plan.
Forward model
mental representation of a movement plan that allows predicting action outcomes by comparing a predicted state

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