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A shared model-based linguistic space for transmitting our thoughts from brain to brain in natural conversations

Zada, Zaid; Goldstein, Ariel; Michelmann, Sebastian; Simony, Erez; Price, Amy; Hasenfratz, Liat; Barham, Emily; Zadbood, Asieh; Doyle, Werner; Friedman, Daniel; Dugan, Patricia; Melloni, Lucia; Devore, Sasha; Flinker, Adeen; Devinsky, Orrin; Nastase, Samuel A; Hasson, Uri
Effective communication hinges on a mutual understanding of word meaning in different contexts. We recorded brain activity using electrocorticography during spontaneous, face-to-face conversations in five pairs of epilepsy patients. We developed a model-based coupling framework that aligns brain activity in both speaker and listener to a shared embedding space from a large language model (LLM). The context-sensitive LLM embeddings allow us to track the exchange of linguistic information, word by word, from one brain to another in natural conversations. Linguistic content emerges in the speaker's brain before word articulation and rapidly re-emerges in the listener's brain after word articulation. The contextual embeddings better capture word-by-word neural alignment between speaker and listener than syntactic and articulatory models. Our findings indicate that the contextual embeddings learned by LLMs can serve as an explicit numerical model of the shared, context-rich meaning space humans use to communicate their thoughts to one another.
PMID: 39096896
ISSN: 1097-4199
CID: 5696672

Neuroecological links of the exposome and One Health

Ibanez, Agustin; Melloni, Lucia; Świeboda, Paweł; Hynes, William; Ikiz, Burcin; Ayadi, Rym; Thioye, Massamba; Walss-Bass, Consuelo; Güntekin, Bahar; Mishra, Jyoti; Salama, Mohamed; Dunlop, Sarah; Duran-Aniotz, Claudia; Eyre, Harris A
This NeuroView assesses the interplay among exposome, One Health, and brain capital in health and disease. Physical and social exposomes affect brain health, and green brain skills are required for environmental health strategies. Ibanez et al. address current gaps and strategies needed in research, policy, and technology, offering a road map for stakeholders.
PMCID:11189719
PMID: 38723637
ISSN: 1097-4199
CID: 5671582

Stable perceptual phenotype of the magnitude of history biases even in the face of global task complexity

Trübutschek, Darinka; Melloni, Lucia
According to a Bayesian framework, visual perception requires active interpretation of noisy sensory signals in light of prior information. One such mechanism, serial dependence, is thought to promote perceptual stability by assimilating current percepts with recent stimulus history. Combining a delayed orientation-adjustment paradigm with predictable (study 1) or unpredictable (study 2) task structure, we test two key predictions of this account in a novel context: first, that serial dependence should persist even in variable environments, and, second, that, within a given observer and context, this behavioral bias should be stable from one occasion to the next. Relying on data of 41 human volunteers and two separate experimental sessions, we confirm both hypotheses. Group-level, attractive serial dependence remained strong even in the face of volatile settings with multiple, unpredictable types of tasks, and, despite considerable interindividual variability, within-subject patterns of attractive and repulsive stimulus-history biases were highly stable from one experimental session to the next. In line with the hypothesized functional role of serial dependence, we propose that, together with previous work, our findings suggest the existence of a more general individual-specific fingerprint with which the past shapes current perception. Congruent with the Bayesian account, interindividual differences may then result from differential weighting of sensory evidence and prior information.
PMCID:10405861
PMID: 37531102
ISSN: 1534-7362
CID: 5594512

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

An adversarial collaboration protocol for testing contrasting predictions of global neuronal workspace and integrated information theory

Melloni, Lucia; Mudrik, Liad; Pitts, Michael; Bendtz, Katarina; Ferrante, Oscar; Gorska, Urszula; Hirschhorn, Rony; Khalaf, Aya; Kozma, Csaba; Lepauvre, Alex; Liu, Ling; Mazumder, David; Richter, David; Zhou, Hao; Blumenfeld, Hal; Boly, Melanie; Chalmers, David J; Devore, Sasha; Fallon, Francis; de Lange, Floris P; Jensen, Ole; Kreiman, Gabriel; Luo, Huan; Panagiotaropoulos, Theofanis I; Dehaene, Stanislas; Koch, Christof; Tononi, Giulio
The relationship between conscious experience and brain activity has intrigued scientists and philosophers for centuries. In the last decades, several theories have suggested different accounts for these relationships. These theories have developed in parallel, with little to no cross-talk among them. To advance research on consciousness, we established an adversarial collaboration between proponents of two of the major theories in the field, Global Neuronal Workspace and Integrated Information Theory. Together, we devised and preregistered two experiments that test contrasting predictions of these theories concerning the location and timing of correlates of visual consciousness, which have been endorsed by the theories' proponents. Predicted outcomes should either support, refute, or challenge these theories. Six theory-impartial laboratories will follow the study protocol specified here, using three complementary methods: Functional Magnetic Resonance Imaging (fMRI), Magneto-Electroencephalography (M-EEG), and intracranial electroencephalography (iEEG). The study protocol will include built-in replications, both between labs and within datasets. Through this ambitious undertaking, we hope to provide decisive evidence in favor or against the two theories and clarify the footprints of conscious visual perception in the human brain, while also providing an innovative model of large-scale, collaborative, and open science practice.
PMCID:9916582
PMID: 36763595
ISSN: 1932-6203
CID: 5426982

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

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