{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T10:05:54Z","timestamp":1782727554947,"version":"3.54.5"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,5,30]],"date-time":"2024-05-30T00:00:00Z","timestamp":1717027200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Hum. Neurosci."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>Understanding the neural correlates of naturalistic behavior is critical for extending and confirming the results obtained from trial-based experiments and designing generalizable brain-computer interfaces that can operate outside laboratory environments. In this study, we aimed to pinpoint consistent spectro-spatial features of neural activity in humans that can discriminate between naturalistic behavioral states.<\/jats:p><\/jats:sec><jats:sec><jats:title>Approach<\/jats:title><jats:p>We analyzed data from five participants using electrocorticography (ECoG) with broad spatial coverage. Spontaneous and naturalistic behaviors such as \u201cTalking\u201d and \u201cWatching TV\u201d were labeled from manually annotated videos. Linear discriminant analysis (LDA) was used to classify the two behavioral states. The parameters learned from the LDA were then used to determine whether the neural signatures driving classification performance are consistent across the participants.<\/jats:p><\/jats:sec><jats:sec><jats:title>Main results<\/jats:title><jats:p>Spectro-spatial feature values were consistently discriminative between the two labeled behavioral states across participants. Mainly, <jats:italic>\u03b8<\/jats:italic>, <jats:italic>\u03b1<\/jats:italic>, and low and high <jats:italic>\u03b3<\/jats:italic> in the postcentral gyrus, precentral gyrus, and temporal lobe showed significant classification performance and feature consistency across participants. Subject-specific performance exceeded 70%. Combining neural activity from multiple cortical regions generally does not improve decoding performance, suggesting that information regarding the behavioral state is non-additive as a function of the cortical region.<\/jats:p><\/jats:sec><jats:sec><jats:title>Significance<\/jats:title><jats:p>To the best of our knowledge, this is the first attempt to identify specific spectro-spatial neural correlates that consistently decode naturalistic and active behavioral states. The aim of this work is to serve as an initial starting point for developing brain-computer interfaces that can be generalized in a realistic setting and to further our understanding of the neural correlates of naturalistic behavior in humans.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnhum.2024.1388267","type":"journal-article","created":{"date-parts":[[2024,5,30]],"date-time":"2024-05-30T12:13:12Z","timestamp":1717071192000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Consistent spectro-spatial features of human ECoG successfully decode naturalistic behavioral states"],"prefix":"10.3389","volume":"18","author":[{"given":"Abdulwahab","family":"Alasfour","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vikash","family":"Gilja","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,5,30]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"112932","DOI":"10.1016\/j.physbeh.2020.112932","article-title":"Decoding covert visual attention based on phase transfer entropy","volume":"222","author":"Ahmadi","year":"2020","journal-title":"Physiol. Behav."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"016021","DOI":"10.1088\/1741-2552\/aaee9c","article-title":"Coarse behavioral context decoding","volume":"16","author":"Alasfour","year":"2019","journal-title":"J. Neural Eng."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"e1010401","DOI":"10.1371\/journal.pcbi.1010401","article-title":"Spatiotemporal dynamics of human high gamma dis-criminate naturalistic behavioral states","volume":"18","author":"Alasfour","year":"2022","journal-title":"PLoS Comput. Biol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1523\/ENEURO.0194-21.2021","article-title":"High \u03b3 activity in cortex and hippocampus is correlated with autonomic tone during sleep","volume":"8","author":"Alasfour","year":"2021","journal-title":"eNeuro"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1126\/science.aav3932","article-title":"Thirst regulates motivated behavior through modulation of brainwide neural population dynamics","volume":"364","author":"Allen","year":"2019","journal-title":"Science"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"036019","DOI":"10.1088\/1741-2552\/ab0c59","article-title":"Publisher: IOP publishing. Speech synthesis from ECoG using densely connected 3d convolutional neural networks","volume":"16","author":"Angrick","year":"2019","journal-title":"J. Neural Eng."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1038\/s41586-019-1119-1","article-title":"Speech synthesis from neural decoding of spoken sentences","volume":"568","author":"Anumanchipalli","year":"2019","journal-title":"Nature"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1016\/s1388-2457(98)00064-9","article-title":"Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks","volume":"110","author":"Aoki","year":"1999","journal-title":"Clin. Neurophysiol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: a practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. S. B."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1038\/s41562-022-01310-0","article-title":"Decoding naturalistic affective behaviour from Spectro-spatial features in multiday human iEEG","volume":"6","author":"Bijanzadeh","year":"2022","journal-title":"Nat. Hum. Behav."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1038\/nature11911","article-title":"Publisher: nature publishing group. Functional organization of human sensorimotor cortex for speech articulation","volume":"495","author":"Bouchard","year":"2013","journal-title":"Nature"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"2040","DOI":"10.1038\/s41593-019-0533-x","article-title":"Publisher: nature research. Unsupervised identification of the internal states that shape natural behavior","volume":"22","author":"Calhoun","year":"2019","journal-title":"Nat. Neurosci."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"2101111","DOI":"10.1109\/JTEHM.2018.2875464","article-title":"Patient-specific pose estimation in clinical environments","volume":"6","author":"Chen","year":"2018","journal-title":"IEEE J. Transl. Eng. Health Med."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1016\/j.jneumeth.2015.01.010","article-title":"Exceeding chance level by chance: the caveat of theoretical chance levels in brain signal classification and statistical assessment of decoding accuracy","volume":"250","author":"Combrisson","year":"2015","journal-title":"J. Neurosci. Methods"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"148756","DOI":"10.1109\/ACCESS.2021.3123098","article-title":"GMMPLS: a novel automatic state-based algorithm for continuous decoding in BMIs","volume":"9","author":"Foodeh","year":"2021","journal-title":"IEEE Access"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"066026","DOI":"10.1088\/1741-2552\/ab355c","article-title":"Neural correlates of unstructured motor behaviors","volume":"16","author":"Gabriel","year":"2019","journal-title":"J. Neural Eng."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"3402","DOI":"10.1109\/EMBC.2016.7591458","article-title":"Neural correlates to automatic behavior estimations from RGB-d video in epilepsy unit","volume":"16","author":"Gabriel","year":"2016","journal-title":"Annu. Int. Conf. IEEE Eng. Med. Biol. Soc"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"7551","DOI":"10.1523\/JNEUROSCI.1920-17.2018","article-title":"Publisher: Society for Neuroscience. Beyond trial-based paradigms: continuous behavior, ongoing neural activity, and natural stimuli","volume":"38","author":"Huk","year":"2018","journal-title":"J. Neurosci."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"056007","DOI":"10.1088\/1741-2560\/7\/5\/056007","article-title":"Decoding spoken words using local field potentials recorded from the cortical surface","volume":"7","author":"Kellis","year":"2010","journal-title":"J. Neural Eng."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1038\/s41593-020-0608-8","article-title":"Machine translation of cortical activity to text with an encoder-decoder framework","volume":"23","author":"Makin","year":"2020","journal-title":"Nat. Neurosci."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1523\/JNEUROSCI.2041-09.2009","article-title":"Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans","volume":"29","author":"Manning","year":"2009","journal-title":"J. Neurosci."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1016\/j.neuroimage.2013.08.070","article-title":"Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations","volume":"85","author":"Miller","year":"2014","journal-title":"New Horiz. Neural Oscillations."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"2424","DOI":"10.1523\/JNEUROSCI.3886-06.2007","article-title":"Spectral changes in cortical surface potentials during motor movement","volume":"27","author":"Miller","year":"2007","journal-title":"J. Neurosci."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"106961","DOI":"10.1016\/j.cmpb.2022.106961","article-title":"Decoding locomotion speed and slope from local field potentials of rat motor cortex","volume":"223","author":"Mirfathollahi","year":"2022","journal-title":"Comput. Methods Prog. Biomed."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"107808","DOI":"10.1016\/j.isci.2023.107808","article-title":"Decoding hand kinetics and kinematics using somatosensory cortex activity in active and passive movement","volume":"26","author":"Mirfathollahi","year":"2023","journal-title":"iScience"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1056\/NEJMoa2027540","article-title":"Neuroprosthesis for decoding speech in a Para-lyzed person with anarthria","volume":"385","author":"Moses","year":"2021","journal-title":"New Eng. J. Med"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1126\/science.1110913","article-title":"Coupling between neuronal firing, field potentials, and fMRI in human auditory cortex","volume":"309","author":"Mukamel","year":"2005","journal-title":"Science"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"66450","DOI":"10.1109\/ACCESS.2021.3076865","article-title":"Single-trial decoding of motion direction during visual attention from local field potential signals","volume":"9","author":"Nazari","year":"2021","journal-title":"IEEE Access"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1038\/s41592-018-0109-9","article-title":"Inferring single-trial neural population dynamics using sequential auto-encoders","volume":"15","author":"Pandarinath","year":"2018","journal-title":"Nat. Methods"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1038\/nature13235","article-title":"Emergence of reproducible spatiotemporal activity during motor learning","volume":"510","author":"Peters","year":"2014","journal-title":"Nature"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1038\/s41597-022-01280-y","article-title":"Publisher: nature publishing group. AJILE12: long-term naturalistic human intracranial neural recordings and pose","volume":"9","author":"Peterson","year":"2022","journal-title":"Sci. Data."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1523\/ENEURO.0007-21.2021","article-title":"Behavioral and neural variability of naturalistic arm movements","volume":"8","author":"Peterson","year":"","journal-title":"eNeuro"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1088\/1741-2552\/abda0b","article-title":"Generalized neural decoders for transfer learning across participants and recording modalities","volume":"18","author":"Peterson","year":"","journal-title":"J. Neural Eng."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"17029","DOI":"10.1038\/s41598-017-17314-0","article-title":"Functional and spatial segregation within the inferior frontal and superior temporal cortices during listening, articulation imagery, and production of vowels","volume":"7","author":"Rampinini","year":"2017","journal-title":"Sci. Rep."},{"key":"ref36","first-page":"APR2016","article-title":"Unsupervised decoding of long-term, naturalistic human neural recordings with automated video and audio annotations","volume":"10","author":"Rao","year":"2016","journal-title":"Front. Hum. Neurosci."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"e1000610","DOI":"10.1371\/journal.pbio.1000610","article-title":"Different origins of gamma rhythm and high-gamma activity in macaque visual cortex","volume":"9","author":"Ray","year":"2011","journal-title":"PLoS Biol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1038\/nbt.4200","article-title":"Mood variations decoded from multi-site intracranial human brain activity","volume":"36","author":"Sani","year":"2018","journal-title":"Nat. Biotechnol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1126\/science.aav7893","article-title":"Spontaneous behaviors drive multidimensional, brainwide activity","volume":"364","author":"Stringer","year":"2019","journal-title":"Science"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"2783","DOI":"10.1109\/TNSRE.2022.3207624","article-title":"An interpretable deep learning model for speech activity detection using Electrocorticographic signals","volume":"30","author":"Stuart","year":"2022","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1038\/s41593-023-01260-4","article-title":"A wearable platform for closed-loop stimulation and recording of single-neuron and local field potential activity in freely moving humans","volume":"26","author":"Topalovic","year":"2023","journal-title":"Nat. Neurosci."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"046011","DOI":"10.1088\/1741-2552\/ab9842","article-title":"Deep learning-based BCI for gait decoding from EEG with LSTM recurrent neural network","volume":"17","author":"Tortora","year":"2020","journal-title":"J. Neural Eng."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnhum.2016.00165","article-title":"Unsupervised decoding of long-term, naturalistic human neural recordings with automated video and audio annotations","volume":"10","author":"Wang","year":"2016","journal-title":"Front. Hum. Neurosci."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1038\/s41586-023-06377-x","article-title":"A high-performance speech neuroprosthesis","volume":"620","author":"Willett","year":"2023","journal-title":"Nature"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1099","DOI":"10.1016\/j.neuron.2018.05.015","article-title":"Publisher: cell press. Unsupervised discovery of demixed, low-dimensional neural dynamics across multiple timescales through tensor component analysis","volume":"98","author":"Williams","year":"2018","journal-title":"Neuron"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"056014","DOI":"10.1088\/1741-2552\/ab2214","article-title":"Dynamic network modeling and dimensionality reduction for human ECoG activity","volume":"16","author":"Yang","year":"2019","journal-title":"J. Neural Eng."},{"key":"ref47","first-page":"5939","article-title":"Electrocorticographic spectral changes associated with ipsilateral individual finger and whole hand movement annual international conference of the IEEE engineering in medicine and biology society","volume":"2008","author":"Zanos","year":"2008","journal-title":"IEEE Eng Med BiolSoc Annu Int Conf"}],"container-title":["Frontiers in Human Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnhum.2024.1388267\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,30]],"date-time":"2024-05-30T12:13:15Z","timestamp":1717071195000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnhum.2024.1388267\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,30]]},"references-count":46,"alternative-id":["10.3389\/fnhum.2024.1388267"],"URL":"https:\/\/doi.org\/10.3389\/fnhum.2024.1388267","relation":{},"ISSN":["1662-5161"],"issn-type":[{"value":"1662-5161","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,30]]},"article-number":"1388267"}}