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

Abstract

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.

Ongoing Brain Activity and Its Role in Cognition: Dual versus Baseline Models

“…Further lines of evidence include: (iv) the rest of the brain's "dark energy" (80-90%) may, by itself, not necessarily or always be accompanied by specific cognitive functions including internally-oriented cognition (Raichle and others., 2001;Raichle and Menon, 2006;Raichle, 2015a and b); (v) involvement of the DMN in externally-oriented cognition like attention to external stimuli (Andrews-Hanna, 2012;Raichle and others., 2001) and complex external naturalistic stimuli others., 2015, 2017;Simony and others., 2016);(vi) DMN and both internally-and externally-oriented cognition in various psychiatric disorders (Anticevic and others., 2012;Northoff and Gomez-Pilar, 2020;Scalabrini and others., 2020).…”

“…Psychiatric disorders like schizophrenia, bipolar disorder (BD), and major depressive disorder (MDD) can be characterized by abnormal shifts in the balance of internally-and externally-oriented cognition. For instance, internally-oriented cognition dominates in schizophrenia delusion and hallucination where it is confused with externally-oriented cognition (Northoff and Gomez-Pilar, 2020). Investigation of GS demonstrated abnormal decreases in GS topography in specifically sensory and motor cortex in schizophrenia while it was abnormally increased in association cortex like prefrontal cortex (Yang and others., 2017) -this may reflect the abnormal shift towards internally-oriented cognition and its confusion with externallyoriented cognition in these patients.…”

“…More indirect support for the blurring between internally-and externally-oriented cognition comes from pathological conditions. Psychiatric disorders like schizophrenia that exhibit changes in the brain's ongoing activity, i.e., resting state, show changes in both internally-and externally-oriented cognition (Ebisch and others., 2018;Northoff and Duncan 2016;Northoff and Gomez-Pilar, 2020). This would not be possible if externally-oriented cognition was not modulated or related in some yet unclear way to the resting state itself.…”

“…Analogously, the spontaneous activity’s shapes task-evoked activity through its degree of scale-freeness (as measured with PLE), which is related to distinct aspects of self-consciousness (Huang and others 2016; Wolff and others 2019a, 2019b; Kolvoort and others 2020; Scalabrini and others 2017), animate social interaction through active touch (Scalabrini and others 2019), multisensory perception (Ferri and others 2015, 2017), and even complex learning chemistry formulae (Bongers and others 2020). Moreover, two recent studies using fMRI and MEG demonstrated that the spontaneous activity’s dynamics (e.g., its power law exponent, delta/alpha power, and oscillatory/fractal components) correlate with the degree of nonadditivity during pre/poststimulus interaction (Aru and others 2019; Huang and others 2017; Wainio-Theberge and others 2020; Wolff and others 2020).…”

“…Even though the dual model seems to be the dominant background assumption in current studies on cognition, it shows some inconsistencies with the empirical data. Various imaging studies using fMRI and EEG/MEG demonstrate that, on the purely neuronal level, spontaneous activity is present in all three: resting state (i.e., the absence of any overt task stimulus), prestimulus activity, and task-related activity (Bolt and others 2017; Cheng and others 2018; Cole and others 2012, 2014, 2016; He 2011; Huang and others 2017; Ito and others 2020; Mennes and others 2010, 2011; Wainio-Theberge and others 2020; Wolff and others 2019a, 2019b, 2020).…”