Does illusory flickering result from rhythmic sampling of visual stimuli?

Approximately a century ago, the oscillatory character of human neural activity was revealed by the discovery of electroencephalographic (EEG) rhythms. Since then, numerous observations have helped to decipher the functional meaning of brain oscillations. Most of the studies have focused on the alpha rhythm (8 –13 Hz), whose strong spectral power is clearly modulated by visual stimulation, visuospatial attention, and working memory load. A robust finding is that alpha power decreases over engaged visual regions (e.g., contralateral to the attended field), whereas alpha power increases over competing regions, pathways, or system modalities. Based on substantial evidence, modern frameworks propose that alpha power decreases reflect active information processing whereas alpha power enhancements reflect top-down inhibition of taskirrelevant regions (Klimesch et al., 2007). On a global scale, alpha-mediated inhibition is an essential part of a gating mechanism by which some areas are disengaged, allowing the allocation of processing resources in task-relevant areas (Jensen and Mazaheri, 2010). On a more local scale, it has an additional aspect: alpha oscillations exert a rhythmic modulation over the excitability of target neural populations (Klimesch et al., 2007). Through this oscillatory mechanism, neuronal activation is more likely at specific phases of the alpha wave, providing controlled timing for cortical processing and communication. Numerous psychophysical reports are compatible with the idea that perception is a discrete process, intrinsically related to the timing of neuronal processes (for review, see VanRullen and Koch, 2003). Curiously, two successive visual events can be interpreted as simultaneous if they are presented within a temporal frame of around 100 ms (Lichtenstein, 1961), a period similar to the alpha cycle. Although a relationship between temporal framing in visual perception and alpha phase is still not clear, recent studies have shown that visual detection threshold fluctuates with the phase of ongoing alpha oscillations (Busch et al., 2009; VanRullen et al., 2011). In addition, cross-correlation analyses of visual stimulation and EEG sequences have shown that random visual flow causes an echo or reverberation of individual alpha oscillatory responses (VanRullen and Macdonald, 2012). Interestingly, removing the alpha frequency components from the stimulation sequence eliminates the EEG alpha echo. Could we be aware of our pulsing perception imposed by the alpha rhythm? This question was addressed by Sokoliuk and VanRullen (2013). These authors introduced a static wheel stimulus based on MacKay rays (MacKay, 1957) that creates a visual illusion of having a regular and cyclic flickering on its center when perceived with the visual periphery. Sokoliuk and VanRullen (2013) propose that the flicker is experienced as a consequence of processing fluctuations caused by the alternation of favorable and unfavorable phases in the alpha wave. In other words, the flickering wheel illusion may allow conscious perception of cortical alpha oscillations. This proposal is based primarily on three observations. The most robust result Sokoliuk and VanRullen (2013) describe is a strong relationship between alpha power modulations and flicker perception. In a smooth pursuit experiment, participants fixated their gaze on a moving dot that revolved around a static, illusory wheel stimulus. The authors observed that the likelihood of flicker detection and occipital alpha power rose and fell together on each revolution of the moving dot. Additionally, the peak frequency of flicker-induced alpha modulations was significantly correlated with the individual alpha frequency. The authors suggest that the flicker illusion is not only the consequence of alpha oscillations, but can also enhance this activity through reverberation mechanisms (VanRullen and Macdonald, 2012). It is not clear, however, whether alpha power enhancements occurred in regions processing the visual stimulus or in reReceived Oct. 21, 2013; revised Nov. 21, 2013; accepted Nov. 25, 2013. M.C.-G. was supported by a grant from the Deutsches Forschungsgemeinschaft (DFG DA1485/1-1). T.H. was supported by a grant from the European Research Council (WIN2CON; ERC StG 283404). We thank Sarang S. Dalal for helpful discussions. Correspondence should be addressed to Maité Crespo-García, Department of Psychology, University of Konstanz, 78457 Konstanz, Germany. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.4486-13.2014 Copyright © 2014 the authors 0270-6474/14/340343-03$15.00/0 The Journal of Neuroscience, January 8, 2014 • 34(2):343–345 • 343