Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling

Raposo, Isabel; Szczepanski, Sara M.; Haaland, Kathleen; Endestad, Tor; Solbakk, Anne-Kristin; Knight, Robert T.; Helfrich, Randolph F.

doi:10.1016/j.cub.2023.09.065

Cited by 4 publications

(2 citation statements)

References 77 publications

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“…One possible mechanism is suggested by previous studies which have linked high alpha/beta power to top-down endogenous signals. A number of studies have substantiated this, linking high alpha/beta power – often arising from the parietal cortex – to attention, imagination, illusory perception, and prediction (Arnal & Giraud, 2012; Auksztulewicz et al, 2017; Bartsch et al, 2015; Bastos et al, 2020; Buschman & Miller, 2007, 2009; De Lange et al, 2013; Engel & Fries, 2010; Fujioka et al, 2012; Hipp et al, 2011; Iversen et al, 2009; Okazaki et al, 2008; Pesaran et al, 2008; Raposo et al, 2023; Sherman et al, 2016; Villena-González et al, 2018). Moreover, previous fMRI studies have reported lower BOLD activity prior to false percepts (Hesselmann et al, 2010; Pajani et al, 2015).…”

Section: Discussionmentioning

confidence: 95%

Shared and diverging neural dynamics underlying false and veridical perception

Haarsma,

Hetenyi,

Kok

2023

Preprint

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We often mistake visual noise for meaningful images, particularly when we strongly expect to see something. For instance, a cat owner might in a poorly lit room mistake a shadowy figure for a cat, due to their expectation to see one. These false percepts can sometimes be as convincing as veridical perception, leading to perceptual judgements of equal confidence. How might seemingly equivalent perceptual judgements occur in the face of such different sensory inputs? One possibility is that while false and veridical percepts are generated by different early sensory processes, subsequent neural mechanisms driving perceptual confidence are identical. To test this possibility, we used MEG to examine the neural mechanisms underlying veridical and false perception with high temporal precision. Participants performed a visual discrimination task requiring them to detect gratings with different orientations under high levels of sensory noise, while on 50% of trials no gratings were presented (noise-only trials). On a subset of noise-only trials, participants reported seeing a grating with high confidence, dubbed here false percepts. We found that high alpha/low beta [11-14Hz] power was increased just before falsely perceiving a grating in noise, but not before veridical percepts, potentially reflecting enhanced reliance on top-down signalling during false percepts. From 250ms post-stimulus, a converging neural signal reflecting perceptual confidence emerged for both absence and presence trials, reflecting an early final common pathway for both veridical and false perceptual inference.Significance statementThe neural mechanisms underlying false percepts are likely different from those that underlie veridical perception, as the former are generated endogenously, whereas the latter are the result of an external stimulus. Yet, false percepts often get confused for veridical perception, suggesting a converging mechanism. This study explores when the neural mechanisms of false and veridical perception diverge and converge. We found that false, but not veridical, percepts were preceded by increased high alpha/low beta [11-14 Hz] power, possibly reflecting a reliance on endogenous signals. From 250ms post-stimulus onwards, there was a converging neural signal reflecting confidence in the percept, shared by veridical and false percepts.

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Section: Discussionmentioning

confidence: 95%

Shared and diverging neural dynamics underlying false and veridical perception

Haarsma,

Hetenyi,

Kok

2023

Preprint

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“…3-D visual space, attention, EEG, rhythmic attentional sampling, time-resolved inverted encoding model which attentional resources are dynamically and periodically navigated between each target over time, a mechanism broadly known as rhythmic attentional sampling (Buschman & Kastner, 2015;Raposo et al, 2023;VanRullen, 2016). For the past decade, rhythmic attentional sampling has received mounting support from converging behavioral and neural findings.…”

Section: Introductionmentioning

confidence: 99%

Concurrent attention to hetero‐depth surfaces in 3‐D visual space is governed by theta rhythm

Deng,

Gao,

et al. 2023

Psychophysiology

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When simultaneously confronted with multiple attentional targets, visual system employs a time‐multiplexing approach in which each target alternates for prioritized access, a mechanism broadly known as rhythmic attentional sampling. For the past decade, rhythmic attentional sampling has received mounting support from converging behavioral and neural findings. However, so compelling are these findings that a critical test ground has been long overshadowed, namely the 3‐D visual space where attention is complicated by extraction of the spatial layout of surfaces extending beyond 2‐D planes. It remains unknown how attentional deployment to multiple targets is accomplished in the 3‐D space. Here, we provided a time‐resolved portrait of the behavioral and neural dynamics when participants concurrently attended to two surfaces defined by motion–depth conjunctions. To characterize the moment‐to‐moment attentional modulation effects, we measured perceptual sensitivity to the hetero‐depth surface motions on a fine temporal scale and reconstructed their neural representations using a time‐resolved multivariate inverted encoding model. We found that the perceptual sensitivity to the two surface motions rhythmically fluctuated over time at ~4 Hz, with one's enhancement closely tracked by the other's diminishment. Moreover, the behavioral pattern was coupled with an ongoing periodic alternation in strength between the two surface motion representations in the same frequency. Together, our findings provide the first converging evidence of an attentional “pendulum” that rhythmically traverses different stereoscopic depth planes and are indicative of a ubiquitous attentional time multiplexor based on theta rhythm in the 3‐D visual space.

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Rhythmic sampling of multiple decision alternatives in the human brain

Siems,

Cao,

Tohidi-Moghaddam

et al. 2023

Preprint

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SummaryDuring decision-making attention plays a pivotal role by guiding information sampling between alternatives. We need to optimally encode different options and compare between them. So far the role of attention in decision-making has only been addressed through saccadic displacements. However, looking is not always attending and attending not always looking. The influence of covert attention on decision-making is poorly understood. Here, we combined a three-alternative perceptual choice task with magnetoencephalography (MEG) recordings to chart covert attention during decision-formation. We found that rhythmic attentional sampling is a neurophysiological mechanism that can temporally disentangle the conflict between focusing and reorienting attention in decision-making. Embedded within an 11Hz oscillation focused processing and reorienting appeared at the peak and trough of the attention oscillation. Reorienting further intrinsically reset the oscillation and covert attention was dissociable from oculomotor activity. We thus propose that (covert) rhythmic sampling is a general cognitive mechanism harnessed to orchestrate flexible information processing in multi-alternative decisions.Highlights‐Assessing covert attention in multi-alternative decision-making with magnetoencephalography (MEG)‐Rhythmic sampling as mechanism orchestrating attention between alternatives‐Focused information sampling alternates with attention switching between decision alternatives‐Covert attention allocation dissociates from oculomotor activity

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Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling

Cited by 4 publications

References 77 publications

Shared and diverging neural dynamics underlying false and veridical perception

Shared and diverging neural dynamics underlying false and veridical perception

Concurrent attention to hetero‐depth surfaces in 3‐D visual space is governed by theta rhythm

Rhythmic sampling of multiple decision alternatives in the human brain

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