Behavioral Oscillations in Attention: Rhythmic α Pulses Mediated through θ Band

Abstract

Neuronal oscillations are ubiquitous in the brain and contribute to perception and attention. However, most associated evidence derives from post hoc correlations between brain dynamics and behavior. Although a few recent studies demonstrate rhythms in behavior, it remains largely unknown whether behavioral performances manifest spectrotemporal dynamics in a neurophysiologically relevant manner (e.g., the temporal modulation of ongoing oscillations, the cross-frequency coupling). To investigate the issue, we examined fine spectrotemporal dynamics of behavioral time courses in a large sample of human participants (n ϭ 49), by taking a high time-resolved psychophysical measurement in a precuing attentional task. We observed compelling dynamic oscillatory patterns directly in behavior. First, typical attentional effects are demonstrated in low-pass (0 -2 Hz) filtered time courses of behavioral responses. Second, an uninformative peripheral cue elicits recurring ␣-band (8 -20 Hz) pulses in behavioral performances, and the elicited ␣ pulses for cued and uncued conditions are in a temporally alternating relationship. Finally, ongoing ␣-band power is phase locked to ongoing -bands (3-5 Hz) in behavioral time courses. Our findings constitute manifestation of oscillations at physiologically relevant rhythms and powerphase locking, as widely observed in neurophysiological recordings, in behavior. The findings suggest that behavioral performance actually consists of rich dynamic information and may reflect underlying neuronal oscillatory substrates. Our data also speak to a neural mechanism for item attention based on successive cycles () of a sequential attentional sampling (␣) process.

Prefrontal cortex modulates posterior alpha oscillations during top-down guided visual perception

“…If the underlying functional brain architecture is inherently rhythmic, then we should be able to observe rhythmic patterns in behavior. This has been recently demonstrated for visual perception (4,5) as well as for highlevel attention (16)(17)(18). Furthermore, neuronal oscillations have been suggested to facilitate sensory predictions and temporal expectations (15,33).…”

“…These observations highlight the need for single trial analyses to better understand the dynamic time course of human cognition (39). We sampled behavioral performance over 850 ms, which does not allow assessing fluctuations below 2 Hz; hence, we speculate that exact frequency might be influenced by the experimental timing (17,18). Brain activity is inherently rhythmic and spans several temporal scales.…”

“…Behavioral performance across all sampled bins was assessed by means of twoway repeated measures ANOVAs with the factors context (predictive/nonpredictive) and rhythmicity (rhythmic/arrhythmic). We focused on hit rates and reaction times in line with previous reports (5,18) to obtain behavioral time courses. We found a significant effect of context (F 1,17 = 17.96, P = 0.0006, η 2 = 0.4687), indicating higher hit rates for predictive than nonpredictive trials ( Fig.…”

“…Importantly, endogenous entrainment does not require rhythmicity in the input stream but reflects an intrinsic mechanism to enable predictions (15). Several studies have demonstrated that visual perception cycles as a function of the alpha phase but only a few reports have demonstrated that multiple rhythms modulate behavior on a fine-grained temporal scale (5,(16)(17)(18)(19).At present, it is uncertain how different temporal scales interact to integrate information and support high-level visual perception. The concept of cross-frequency coupling (CFC), where the phase of a low-frequency oscillation modulates the amplitude of a faster oscillation, may constitute a key element for spatiotemporal organization in the human cortex (20) but has several methodological limitations that must be considered (21-23).…”

“…Importantly, endogenous entrainment does not require rhythmicity in the input stream but reflects an intrinsic mechanism to enable predictions (15). Several studies have demonstrated that visual perception cycles as a function of the alpha phase but only a few reports have demonstrated that multiple rhythms modulate behavior on a fine-grained temporal scale (5,(16)(17)(18)(19).…”