Attention Periodically Binds Visual Features As Single Events Depending on Neural Oscillations Phase-Locked to Action

Abstract

Recent psychophysical studies have demonstrated that periodic attention in the 4-8 Hz range facilitates performance on visual detection. The present study examined the periodicity of feature binding, another major function of attention, in human observers (3 females and 5 males for behavior, with 7 males added for the EEG experiment). In a psychophysical task, observers reported a synchronous pair of brightness (light/dark) and orientation (clockwise/counterclockwise) patterns from two combined brightness-orientation pairs presented in rapid succession. We found that temporal binding performance exhibits periodic oscillations at ϳ8 Hz as a function of stimulus onset delay from a self-initiated button press in conditions where brightness-orientation pairs were spatially separated. However, as one would expect from previous studies on pre-attentive binding, significant oscillations were not apparent in conditions where brightnessorientation pairs were spatially superimposed. EEG results, while fully compatible with behavioral oscillations, also revealed a significant dependence of binding performance across trials on prestimulus neural oscillatory phases within the corresponding band. The peak frequency of this dependence was found to be correlated with intertrial phase coherence (ITPC) around the timing of button press in parietal sensors. Moreover, the peak frequency of the ITPC was found to predict behavioral frequency in individual observers. Together, these results suggest that attention operates periodically (at ϳ8 Hz) on the perceptual binding of multimodal visual information and is mediated by neural oscillations phase-locked to voluntary action.

A New Unifying Account of the Roles of Neuronal Entrainment

“…Although this is yet to be demonstrated in invasive experiments, human EEG and ECoG studies indicate that when entrainment occurs (likely most if not all of the time), it is widespread across the brain as expected based on its supramodality property (Box 3). Thus, entrainment is an ideal candidate mechanism for predictively aligning neuronal oscillations to certain phases across distinct brain regions, resulting in communication through coherence [41,161], and binding of sensory information [173][174][175] if high excitability phases are matched, and resulting in disconnection through coherence if these phases are mismatched. This latter mechanism is very important, as it prevents the passage of inputs to higher order cortices during times when entrained oscillations in non-attentional-spotlight regions are at their high excitability phases.…”

Visual sensitivity and bias oscillate phase-locked to saccadic eye movements

“…A growing body of scientific literature shows that perceptual rhythmic oscillations are also synchronized with voluntary actions, and this synchronization can modulate several visual functions including visual contrast discrimination of salient stimuli (Benedetto & Morrone, 2017;Benedetto, Morrone, & Tomassini, 2019;Benedetto, Spinelli, & Morrone, 2016;Tomassini, Spinelli, Jacono, Sandini, & Morrone, 2015), visual attention (Hogendoorn, 2016), feature binding (Nakayama & Motoyoshi, 2019), and temporal integra-tion\segregation (Wutz, Muschter, van Koningsbruggen, Weisz, & Melcher, 2016). Consistent with the hypothesis of a strong link between sensorimotor integration and neural oscillations, it has been demonstrated that the phase of neural oscillations can predict reaction-time to perceptual events (Drewes & VanRullen, 2011;Lansing, 1957;Surwillo, 1961), and that a transient visual response can reset the phase of low-frequency tremor oscillations in peripheral muscles (Wood, Gu, Corneil, Gribble, & Goodale, 2015).…”

Attention Samples Items in Visual Working Memory Rhythmically

“…Specifically the effects of accuracy indicate that color-based retrieval also led to a prioritization of the orientation associated with that item. As mentioned before, the multiplexing of several multi-feature representations in working memory might serve to discretely separate features belonging to one items and features belonging to another item (Hitch et al, 2020; Nakayama & Motoyoshi, 2019; Treisman, 1996). Our study supports this claim by showing that items which are prioritized via their color feature show a facilitation of probe comparisons based on their orientation feature.…”