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Spatiotemporal dynamics of human high gamma discriminate naturalistic behavioral states

Alasfour, Abdulwahab; Gabriel, Paolo; Jiang, Xi; Shamie, Isaac; Melloni, Lucia; Thesen, Thomas; Dugan, Patricia; Friedman, Daniel; Doyle, Werner; Devinsky, Orin; Gonda, David; Sattar, Shifteh; Wang, Sonya; Halgren, Eric; Gilja, Vikash
In analyzing the neural correlates of naturalistic and unstructured behaviors, features of neural activity that are ignored in a trial-based experimental paradigm can be more fully studied and investigated. Here, we analyze neural activity from two patients using electrocorticography (ECoG) and stereo-electroencephalography (sEEG) recordings, and reveal that multiple neural signal characteristics exist that discriminate between unstructured and naturalistic behavioral states such as "engaging in dialogue" and "using electronics". Using the high gamma amplitude as an estimate of neuronal firing rate, we demonstrate that behavioral states in a naturalistic setting are discriminable based on long-term mean shifts, variance shifts, and differences in the specific neural activity's covariance structure. Both the rapid and slow changes in high gamma band activity separate unstructured behavioral states. We also use Gaussian process factor analysis (GPFA) to show the existence of salient spatiotemporal features with variable smoothness in time. Further, we demonstrate that both temporally smooth and stochastic spatiotemporal activity can be used to differentiate unstructured behavioral states. This is the first attempt to elucidate how different neural signal features contain information about behavioral states collected outside the conventional experimental paradigm.
PMID: 35939509
ISSN: 1553-7358
CID: 5286572

Advances in human intracranial electroencephalography research, guidelines and good practices

Mercier, Manuel R; Dubarry, Anne-Sophie; Tadel, François; Avanzini, Pietro; Axmacher, Nikolai; Cellier, Dillan; Vecchio, Maria Del; Hamilton, Liberty S; Hermes, Dora; Kahana, Michael J; Knight, Robert T; Llorens, Anais; Megevand, Pierre; Melloni, Lucia; Miller, Kai J; Piai, Vitória; Puce, Aina; Ramsey, Nick F; Schwiedrzik, Caspar M; Smith, Sydney E; Stolk, Arjen; Swann, Nicole C; Vansteensel, Mariska J; Voytek, Bradley; Wang, Liang; Lachaux, Jean-Philippe; Oostenveld, Robert
Since the second-half of the twentieth century, intracranial electroencephalography (iEEG), including both electrocorticography (ECoG) and stereo-electroencephalography (sEEG), has provided an intimate view into the human brain. At the interface between fundamental research and the clinic, iEEG provides both high temporal resolution and high spatial specificity but comes with constraints, such as the individual's tailored sparsity of electrode sampling. Over the years, researchers in neuroscience developed their practices to make the most of the iEEG approach. Here we offer a critical review of iEEG research practices in a didactic framework for newcomers, as well addressing issues encountered by proficient researchers. The scope is threefold: (i) review common practices in iEEG research, (ii) suggest potential guidelines for working with iEEG data and answer frequently asked questions based on the most widespread practices, and (iii) based on current neurophysiological knowledge and methodologies, pave the way to good practice standards in iEEG research. The organization of this paper follows the steps of iEEG data processing. The first section contextualizes iEEG data collection. The second section focuses on localization of intracranial electrodes. The third section highlights the main pre-processing steps. The fourth section presents iEEG signal analysis methods. The fifth section discusses statistical approaches. The sixth section draws some unique perspectives on iEEG research. Finally, to ensure a consistent nomenclature throughout the manuscript and to align with other guidelines, e.g., Brain Imaging Data Structure (BIDS) and the OHBM Committee on Best Practices in Data Analysis and Sharing (COBIDAS), we provide a glossary to disambiguate terms related to iEEG research.
PMID: 35792291
ISSN: 1095-9572
CID: 5280362

Tracking transitional probabilities and segmenting auditory sequences are dissociable processes in adults and neonates

Benjamin, Lucas; Fló, Ana; Palu, Marie; Naik, Shruti; Melloni, Lucia; Dehaene-Lambertz, Ghislaine
Since speech is a continuous stream with no systematic boundaries between words, how do pre-verbal infants manage to discover words? A proposed solution is that they might use the transitional probability between adjacent syllables, which drops at word boundaries. Here, we tested the limits of this mechanism by increasing the size of the word-unit to four syllables, and its automaticity by testing asleep neonates. Using markers of statistical learning in neonates' EEG, compared to adult behavioral performances in the same task, we confirmed that statistical learning is automatic enough to be efficient even in sleeping neonates. We also revealed that: (1) Successfully tracking transition probabilities (TP) in a sequence is not sufficient to segment it. (2) Prosodic cues, as subtle as subliminal pauses, enable to recover words segmenting capacities. (3) Adults' and neonates' capacities to segment streams seem remarkably similar despite the difference of maturation and expertise. Finally, we observed that learning increased the overall similarity of neural responses across infants during exposure to the stream, providing a novel neural marker to monitor learning. Thus, from birth, infants are equipped with adult-like tools, allowing them to extract small coherent word-like units from auditory streams, based on the combination of statistical analyses and auditory parsing cues. RESEARCH HIGHLIGHTS: Successfully tracking transitional probabilities in a sequence is not always sufficient to segment it. Word segmentation solely based on transitional probability is limited to bi- or tri-syllabic elements. Prosodic cues, as subtle as subliminal pauses, enable to recover chunking capacities in sleeping neonates and awake adults for quadriplets.
PMID: 35772033
ISSN: 1467-7687
CID: 5281302

Statistical learning in patients in the minimally conscious state

Xu, Chuan; Li, Hangcheng; Gao, Jiaxin; Li, Lingling; He, Fangping; Yu, Jie; Ling, Yi; Gao, Jian; Li, Jingqi; Melloni, Lucia; Luo, Benyan; Ding, Nai
When listening to speech, cortical activity can track mentally constructed linguistic units such as words, phrases, and sentences. Recent studies have also shown that the neural responses to mentally constructed linguistic units can predict the outcome of patients with disorders of consciousness (DoC). In healthy individuals, cortical tracking of linguistic units can be driven by both long-term linguistic knowledge and online learning of the transitional probability between syllables. Here, we investigated whether statistical learning could occur in patients in the minimally conscious state (MCS) and patients emerged from the MCS (EMCS) using electroencephalography (EEG). In Experiment 1, we presented to participants an isochronous sequence of syllables, which were composed of either 4 real disyllabic words or 4 reversed disyllabic words. An inter-trial phase coherence analysis revealed that the patient groups showed similar word tracking responses to real and reversed words. In Experiment 2, we presented trisyllabic artificial words that were defined by the transitional probability between words, and a significant word-rate EEG response was observed for MCS patients. These results suggested that statistical learning can occur with a minimal conscious level. The residual statistical learning ability in MCS patients could potentially be harnessed to induce neural plasticity.
PMID: 35670595
ISSN: 1460-2199
CID: 5248292

The ConTraSt database for analysing and comparing empirical studies of consciousness theories

Yaron, Itay; Melloni, Lucia; Pitts, Michael; Mudrik, Liad
Understanding how consciousness arises from neural activity remains one of the biggest challenges for neuroscience. Numerous theories have been proposed in recent years, each gaining independent empirical support. Currently, there is no comprehensive, quantitative and theory-neutral overview of the field that enables an evaluation of how theoretical frameworks interact with empirical research. We provide a bird's eye view of studies that interpreted their findings in light of at least one of four leading neuroscientific theories of consciousness (N = 412 experiments), asking how methodological choices of the researchers might affect the final conclusions. We found that supporting a specific theory can be predicted solely from methodological choices, irrespective of findings. Furthermore, most studies interpret their findings post hoc, rather than a priori testing critical predictions of the theories. Our results highlight challenges for the field and provide researchers with an open-access website ( https://ContrastDB.tau.ac.il ) to further analyse trends in the neuroscience of consciousness.
PMID: 35190711
ISSN: 2397-3374
CID: 5175042

Shared computational principles for language processing in humans and deep language models

Goldstein, Ariel; Zada, Zaid; Buchnik, Eliav; Schain, Mariano; Price, Amy; Aubrey, Bobbi; Nastase, Samuel A; Feder, Amir; Emanuel, Dotan; Cohen, Alon; Jansen, Aren; Gazula, Harshvardhan; Choe, Gina; Rao, Aditi; Kim, Catherine; Casto, Colton; Fanda, Lora; Doyle, Werner; Friedman, Daniel; Dugan, Patricia; Melloni, Lucia; Reichart, Roi; Devore, Sasha; Flinker, Adeen; Hasenfratz, Liat; Levy, Omer; Hassidim, Avinatan; Brenner, Michael; Matias, Yossi; Norman, Kenneth A; Devinsky, Orrin; Hasson, Uri
Departing from traditional linguistic models, advances in deep learning have resulted in a new type of predictive (autoregressive) deep language models (DLMs). Using a self-supervised next-word prediction task, these models generate appropriate linguistic responses in a given context. In the current study, nine participants listened to a 30-min podcast while their brain responses were recorded using electrocorticography (ECoG). We provide empirical evidence that the human brain and autoregressive DLMs share three fundamental computational principles as they process the same natural narrative: (1) both are engaged in continuous next-word prediction before word onset; (2) both match their pre-onset predictions to the incoming word to calculate post-onset surprise; (3) both rely on contextual embeddings to represent words in natural contexts. Together, our findings suggest that autoregressive DLMs provide a new and biologically feasible computational framework for studying the neural basis of language.
PMCID:8904253
PMID: 35260860
ISSN: 1546-1726
CID: 5190382

Event boundaries shape temporal organization of memory by resetting temporal context

Pu, Yi; Kong, Xiang-Zhen; Ranganath, Charan; Melloni, Lucia
In memory, our continuous experiences are broken up into discrete events. Boundaries between events are known to influence the temporal organization of memory. However, how and through which mechanism event boundaries shape temporal order memory (TOM) remains unknown. Across four experiments, we show that event boundaries exert a dual role: improving TOM for items within an event and impairing TOM for items across events. Decreasing event length in a list enhances TOM, but only for items at earlier local event positions, an effect we term the local primacy effect. A computational model, in which items are associated to a temporal context signal that drifts over time but resets at boundaries captures all behavioural results. Our findings provide a unified algorithmic mechanism for understanding how and why event boundaries affect TOM, reconciling a long-standing paradox of why both contextual similarity and dissimilarity promote TOM.
PMID: 35110527
ISSN: 2041-1723
CID: 5153662

On Keeping Our Adversaries Close, Preventing Collateral Damage, and Changing Our Minds

Melloni, Lucia
Disagreement is a powerful engine of scientific advance. It sharpens conceptual boundaries, directs attention to neglected issues, and, of course, prompts the design of would-be decisive experiments"”(Gilovich et al., 1998)
SCOPUS:85131320956
ISSN: 2211-3681
CID: 5314622

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

Iemi, Luca; Gwilliams, Laura; Samaha, Jason; Auksztulewicz, Ryszard; Cycowicz, Yael M; King, Jean-Remi; Nikulin, Vadim V; Thesen, Thomas; Doyle, Werner; Devinsky, Orrin; Schroeder, Charles E; Melloni, Lucia; Haegens, Saskia
The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.
PMID: 34875382
ISSN: 1095-9572
CID: 5105842

Long-term priors influence visual perception through recruitment of long-range feedback

Hardstone, Richard; Zhu, Michael; Flinker, Adeen; Melloni, Lucia; Devore, Sasha; Friedman, Daniel; Dugan, Patricia; Doyle, Werner K; Devinsky, Orrin; He, Biyu J
Perception results from the interplay of sensory input and prior knowledge. Despite behavioral evidence that long-term priors powerfully shape perception, the neural mechanisms underlying these interactions remain poorly understood. We obtained direct cortical recordings in neurosurgical patients as they viewed ambiguous images that elicit constant perceptual switching. We observe top-down influences from the temporal to occipital cortex, during the preferred percept that is congruent with the long-term prior. By contrast, stronger feedforward drive is observed during the non-preferred percept, consistent with a prediction error signal. A computational model based on hierarchical predictive coding and attractor networks reproduces all key experimental findings. These results suggest a pattern of large-scale information flow change underlying long-term priors' influence on perception and provide constraints on theories about long-term priors' influence on perception.
PMID: 34725348
ISSN: 2041-1723
CID: 5037932