A dual role of prestimulus spontaneous neural activity in visual object recognition

Podvalny, Ella; Flounders, Matthew W.; King, Leana E; Holroyd, Tom; He, Biyu J.

doi:10.1038/s41467-019-11877-4

Cited by 69 publications

(79 citation statements)

References 71 publications

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“…These results demonstrate that pre-stimulus activity modulates the degree of category tuning on the trial-by-trial basis in category-selective areas of the cortex. Previous studies have mainly focused on the overall correlation between the pre-stimulus activity and the evoked response in features including phase and oscillatory power of the event-related response 23 – 25 , often not definitively localized to the regions that process the stimulus class being presented 41 . The results here demonstrate that pre-stimulus activity modulates the post-stimulus activity in the regions that are selective for the stimulus being viewed.…”

Section: Discussionmentioning

confidence: 99%

Endogenous activity modulates stimulus and circuit-specific neural tuning and predicts perceptual behavior

Ward

Richardson

et al. 2020

Nat Commun

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Perception reflects not only sensory inputs, but also the endogenous state when these inputs enter the brain. Prior studies show that endogenous neural states influence stimulus processing through non-specific, global mechanisms, such as spontaneous fluctuations of arousal. It is unclear if endogenous activity influences circuit and stimulus-specific processing and behavior as well. Here we use intracranial recordings from 30 pre-surgical epilepsy patients to show that patterns of endogenous activity are related to the strength of trial-by-trial neural tuning in different visual category-selective neural circuits. The same aspects of the endogenous activity that relate to tuning in a particular neural circuit also correlate to behavioral reaction times only for stimuli from the category that circuit is selective for. These results suggest that endogenous activity can modulate neural tuning and influence behavior in a circuit- and stimulus-specific manner, reflecting a potential mechanism by which endogenous neural states facilitate and bias perception.

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Section: Discussionmentioning

confidence: 99%

Endogenous activity modulates stimulus and circuit-specific neural tuning and predicts perceptual behavior

Ward

Richardson

et al. 2020

Nat Commun

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“…There is increasing appreciation of the relationship between arousal, pupil size, and cognitive performance [15][16][17][18][19]. For example, unlike spatial attention, which increases perceptual sensitivity in a local region in visual space, changes in arousal lead to pupil dilation and do not necessarily increase sensitivity [15,20,21]. If this hypothesis is correct, then task-related hemodynamic activity may contain important information about cognitive processes, which is overlooked by the vast majority of fMRI experiments.…”

Section: Introductionmentioning

confidence: 99%

Task-related activity in human visual cortex

2020

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The brain exhibits widespread endogenous responses in the absence of visual stimuli, even at the earliest stages of visual cortical processing. Such responses have been studied in monkeys using optical imaging with a limited field of view over visual cortex. Here, we used functional MRI (fMRI) in human participants to study the link between arousal and endogenous responses in visual cortex. The response that we observed was tightly entrained to task timing, was spatially extensive, and was independent of visual stimulation. We found that this response follows dynamics similar to that of pupil size and heart rate, suggesting that task-related activity is related to arousal. Finally, we found that higher reward increased response amplitude while decreasing its trial-to-trial variability (i.e., the noise). Computational simulations suggest that increased temporal precision underlies both of these observations. Our findings are consistent with optical imaging studies in monkeys and support the notion that arousal increases precision of neural activity.

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“…György Buszáki (Buzsáki, 2019) suggests an alternative approach, ‘inside-out’; unlike the traditional ‘outside-in’, it places intrinsic neural activity as a key factor (inside) in modulating activity change related to external stimuli (outside) (see also Northoff et al 2010, Northoff 2014a and b). Consistent with this approach (Buzsáki, 2019), studies (He, 2013; Baria et al, 2017; Huang et al, 2017; Nieus et al, 2018; Galindo-Leon et al, 2019; Hirschmann et al, 2019; Podvalny et al, 2019) have demonstrated that poststimulus activity levels depend on the initial state, the level of prestimulus activity (Yamagishi et al, 2008; Mathewson et al, 2009; Northoff et al, 2010; Fellinger et al, 2011; Hanslmayr et al, 2013; He, 2013; Milton and Pleydell-Pearce, 2016; Benwell et al, 2017; Huang et al, 2017; Hirschmann et al, 2019). These findings demand the question: how and in what way do prestimulus activity levels shape stimulus-induced activity beyond the external stimulus?…”

Section: Introductionmentioning

confidence: 72%

The hybrid nature of task-evoked activity: Inside-out neural dynamics in intracranial EEG and Deep Learning

Wolff

Chen

Tumati

et al. 2020

Preprint

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A.AbstractThe standard approach in neuroscience research infers from the external stimulus (outside) to the brain (inside) through stimulus-evoked activity. Recently challenged by Buzsáki, he advocates the reverse; an inside-out approach inferring from the brain’s activity to the neural effects of the stimulus. If so, stimulus-evoked activity should be a hybrid of internal and external components. Providing direct evidence for this hybrid nature, we measured human intracranial stereo-electroencephalography (sEEG) to investigate how prestimulus variability, i.e., standard deviation, shapes poststimulus activity through trial-to-trial variability. We first observed greater poststimulus variability quenching in trials exhibiting high prestimulus variability. Next, we found that the relative effect of the stimulus was higher in the later (300-600ms) than the earlier (0-300ms) poststimulus period. These results were extended by our Deep Learning LSTM network models at the single trial level. The accuracy to classify single trials (prestimulus low/high) increased greatly when the models were trained and tested with real trials compared to trials that exclude the effects of the prestimulus-related ongoing dynamics (corrected trials). Lastly, we replicated our findings showing that trials with high prestimulus variability in theta and alpha bands exhibits faster reaction times. Together, our results support the inside-out approach by demonstrating that stimulus-related activity is a hybrid of two factors: 1) the effects of the external stimulus itself, and 2) the effects of the ongoing dynamics spilling over from the prestimulus period, with the second, i.e., the inside, dwarfing the influence of the first, i.e., the outside.B.Significance StatementOur findings signify a significant conceptual advance in the relationship between pre- and poststimulus dynamics in humans. These findings are important as they show that we miss an essential component - the impact of the ongoing dynamics - when restricting our analyses to the effects of the external stimulus alone. Consequently, these findings may be crucial to fully understand higher cognitive functions and their impairments, as can be seen in psychiatric illnesses. In addition, our Deep Learning LSTM models show a second conceptual advance: high classification accuracy of a single trial to its prestimulus state. Finally, our replicated results in an independent dataset and task showed that this relationship between pre- and poststimulus dynamics exists across tasks and is behaviorally relevant.

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A dual role of prestimulus spontaneous neural activity in visual object recognition

Cited by 69 publications

References 71 publications

Endogenous activity modulates stimulus and circuit-specific neural tuning and predicts perceptual behavior

Endogenous activity modulates stimulus and circuit-specific neural tuning and predicts perceptual behavior

Task-related activity in human visual cortex

The hybrid nature of task-evoked activity: Inside-out neural dynamics in intracranial EEG and Deep Learning

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