Brain oscillations in perception, timing and action

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Highlights

  • The multidimensional processing of information in the brain occurs through the coupling of multiple local circuits.

  • The main neural underpinning of the multidimensional processing of information is cross-frequency phase-amplitude coupling.

  • Coupling between perception and action determines the outcome of sensorimotor tasks.

Catching a thrown ball requires a tight coupling between perception and motor control. In this review, we examine multidimensional information processing across various perceptual and motor tasks. We summarize how perception, timing and action can be understood in terms of the coupling of gamma band oscillations, which represent the local activities of brain circuits, to a specific phase of long-range low-frequency oscillations. We propose a temporal window of integration that emerges from cross-frequency coupling that serves to produce optimized action.

Introduction

To hit a pitched baseball requires that the batter generates accurate estimates of the position, speed, and timing of the moving ball and use this information to produce a coordinated movement. Humans are adept in compensating for their own sensorimotor uncertainty in the execution of skilled actions [1, 2••, 3]; however, the neural mechanisms underlying the temporal coordination between perception and action have not been fully established.

Different lines of evidence have facilitated our understanding of the computations and physiological underpinnings that are involved in the coupling of perception and action. For example, a recent computational modeling study revealed that the internal representations of observers’ spatial visuomotor errors (in visuomotor decision tasks) are best described by a mixture of distributions that differ in location and scale [2••]. This indicates that the internal probability density functions of their own visuomotor error distributions are discrete [2••]. These results suggest that discrete neurophysiological processes may be responsible for various sensorimotor tasks. In this review, we propose that the processing of multidimensional information by neuronal populations occurs in separate epochs and that these epochs represent different facets of the interaction between perception and action (Figure 1).

Section snippets

Multidimensional processing of sensorimotor information

Over the last decade, there has been considerable interest in the roles of cross-frequency phase-amplitude coupling in various cognitive functions [4••]. Cross-frequency phase-amplitude coupling is a phenomenon in which the phase of a lower frequency brain oscillation modulates the amplitudes, i.e., the differences in the maxima and minima of oscillation waves, of a higher frequency oscillation to create ‘packets’ of those higher frequency waves [4••]. Coupling of the phases of low-frequency

Multidimensional processing in apparent visual motion

In this section, we argue that pre-stimulus alpha power and spontaneous brain oscillations influence apparent motion perception [37]. Apparent motion is a visual illusion in which motion is perceived when two spatially distinct static objects alternate in sequence. Apparent motion illusions are robust at presentation frequencies of approximately 3 Hz. Apparent motion has been deemed to be dependent on the ability to use predictive feedback signals in the processing of ‘fragmented’ sensory

Multidimensional processing in timing and action

Phase-amplitude coupling provides a plausible mechanism for the calibration of modular clocks. This calibration involves endogenous oscillators within various networks, modules that calibrate the oscillators, and downstream circuits that process task-specific time intervals. These components are connected via flexible connections as proposed by Gupta (2014) [40]. The modular clock mechanism is calibrated by circuits, such as those in the cerebellum and posterior parietal cortex, which are

Summary

VanRullen and Koch (2003) proposed that cross-frequency interactions between gamma and alpha oscillations constrain perception [51]. We extend this proposal to include motor functions to understand the role of the multidimensional processing of information during sensorimotor tasks. The multidimensional processing provides an important basis for understanding how different circuits of the brain can be temporally coupled during various sensorimotor tasks.

Conflict of interest statement

Nothing declared.

Acknowledgements

This study was supported by grants from the Natural Science Foundation of China (31200760), the National High Technology Research and Development Program of China (863 Program, 2012AA011602) and the Fund for Fostering Talents in Basic Science (J1103602) to LC. DSG would like to acknowledge his gratitude to the students, faculty and staff of Camden County College, New Jersey, USA and the ResearchGate™ community.

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