Binding Mechanisms in Visual Perception and Their Link With Neural Oscillations: A Review of Evidence From tACS.

Andrea Ghiani,Marcello Maniglia,Luca Ronconi,David Melcher,Luca Battaglini

doi:10.3389/fpsyg.2021.643677

Abstract

Neurophysiological studies in humans employing magneto- (MEG) and electro- (EEG) encephalography increasingly suggest that oscillatory rhythmic activity of the brain may be a core mechanism for binding sensory information across space, time, and object features to generate a unified perceptual representation. To distinguish whether oscillatory activity is causally related to binding processes or whether, on the contrary, it is a mere epiphenomenon, one possibility is to employ neuromodulatory techniques such as transcranial alternating current stimulation (tACS). tACS has seen a rising interest due to its ability to modulate brain oscillations in a frequency-dependent manner. In the present review, we critically summarize current tACS evidence for a causal role of oscillatory activity in spatial, temporal, and feature binding in the context of visual perception. For temporal binding, the emerging picture supports a causal link with the power and the frequency of occipital alpha rhythms (8–12 Hz); however, there is no consistent evidence on the causal role of the phase of occipital tACS. For feature binding, the only study available showed a modulation by occipital alpha tACS. The majority of studies that successfully modulated oscillatory activity and behavioral performance in spatial binding targeted parietal areas, with the main rhythms causally linked being the theta (~7 Hz) and beta (~18 Hz) frequency bands. On the other hand, spatio-temporal binding has been directly modulated by parieto-occipital gamma (~40–60 Hz) and alpha (10 Hz) tACS, suggesting a potential role of cross-frequency coupling when binding across space and time. Nonetheless, negative or partial results have also been observed, suggesting methodological limitations that should be addressed in future research. Overall, the emerging picture seems to support a causal role of brain oscillations in binding processes and, consequently, a certain degree of plasticity for shaping binding mechanisms in visual perception, which, if proved to have long lasting effects, can find applications in different clinical populations.

Highlights

To build a representation of the incoming sensory flow, our brain needs to bind sensory information in a meaningful way, giving rise to a clear and smooth perception of the world
Even if correlational studies showed a possible role of alpha activity in perceptual switch rates (Strüber and Herrmann, 2002; Mathes et al, 2010), this study found a causal link of low gamma activity only, highlighting the advantage of transcranial alternating current stimulation (tACS) in identifying brain oscillations that are causally relevant for binding processes during ambiguous stimulation
The goal of this review was to provide a comprehensive picture of current evidence regarding the potential causal role of brain oscillations in binding processes, both in the temporal and spatial domain, in light of previous neurophysiological research that linked several binding mechanisms to precise oscillatory correlates (e.g., Varela et al, 1981; Rose and Büchel, 2005; Busch and VanRullen, 2010; Jensen et al, 2012; Hanslmayr et al, 2013; McLelland et al, 2016; Wutz et al, 2016, 2018; for reviews see VanRullen, 2016; Costa et al, 2017; Ronconi et al, 2017; White, 2018)

Summary

INTRODUCTION

To build a representation of the incoming sensory flow, our brain needs to bind sensory information in a meaningful way, giving rise to a clear and smooth perception of the world. Recent studies showed that (quasi) discrete temporal windows of integration, as measured by a two-flash fusion task, depend on the frequency (speed) (Samaha and Postle, 2015) and phase (Ronconi et al, 2017) of parieto-occipital EEG alpha activity In their task, participants were shown two sequential flashes, with an increase in the time interval between the flashes generally leading to a switch in perception from one to two unique stimulus events (Figure 1B). Ronconi and Melcher found a phase-dependent modulation of segregation/integration performance after sensory entrainment in the alpha and theta frequency, suggesting a role of both frequencies in segregating/integrating stimuli across the temporal domain (Ronconi and Melcher, 2017) Given this evidence, one may expect to find tACS studies that aimed to modulate theta activity to investigate its potential causal role in temporal binding. Starting from this correlational evidence, Stonkus et al tested a causal role of these theta oscillations in a similar contour integration task

References tACS

10 Hz tACS did not selectively increase alpha power after stimulation

18 Hz tACS selectively increased beta power after stimulation

CONCLUSIONS AND FUTURE DIRECTIONS