Recognition memory is the ability to recognize previously encountered objects. Even this relatively simple, yet extremely fast, ability requires the coordinated activity of large-scale brain networks. However, little is known about the sub-second dynamics of these networks. The majority of current studies into large-scale network dynamics is primarily based on imaging techniques suffering from either poor temporal or spatial resolution. We investigated the dynamics of large-scale functional brain networks underlying recognition memory at the millisecond scale. Specifically, we analyzed dynamic effective connectivity from intracranial electroencephalography while epileptic subjects (n = 18) performed a fast visual recognition memory task. Our data-driven investigation using Granger causality and the analysis of communities with the Louvain algorithm spotlighted a dynamic interplay of two large-scale networks associated with successful recognition. The first network involved the right visual ventral stream and bilateral frontal regions. It was characterized by early, predominantly bottom-up information flow peaking at 115 ms. It was followed by the involvement of another network with predominantly top-down connectivity peaking at 220 ms, mainly in the left anterior hemisphere. The transition between these two networks was associated with changes in network topology, evolving from a more segregated to a more integrated state. These results highlight that distinct large-scale brain networks involved in visual recognition memory unfold early and quickly, within the first 300 ms after stimulus onset. Our study extends the current understanding of the rapid network changes during rapid cognitive processes.

Centre de Recherche Cerveau et Cognition Toulouse 3 University CNRS UMR 5549 Toulouse France

Department of Computing and Control Engineering University of Chemistry and Technology Prague Czech Republic

Institute of Computer Science of the Czech Academy of Sciences Prague Czech Republic

National Institute of Mental Health Klecany Czech Republic

Toulouse NeuroImaging Center Toulouse France

University Hospital Purpan Toulouse France

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Aggleton, J. P. , & Brown, M. W. (1999). Episodic memory, amnesia, and the hippocampal‐anterior thalamic axis. Behavioral and Brain Sciences, 22(3), 425–444. 10.1017/s0140525x99002034 PubMed DOI

Bar, M. , Kassam, K. S. , Ghuman, A. S. , Boshyan, J. , Schmid, A. M. , Dale, A. M. , Hämäläinen, M. S. , Marinkovic, K. , Schacter, D. L. , Rosen, B. R. , & Halgren, E. (2006). Top‐down facilitation of visual recognition. Proceedings of the National Academy of Sciences, 103, 449–454. 10.1073/pnas.0507062103 PubMed DOI PMC

Barbeau, E. J. , Chauvel, P. , Moulin, C. J. A. , Regis, J. , & Liégeois‐Chauvel, C. (2017). Hippocampus duality: Memory and novelty detection are subserved by distinct mechanisms. Hippocampus, 27, 405–416. 10.1002/hipo.22699 PubMed DOI

Barbeau, E. J. , Taylor, M. J. , Regis, J. , Marquis, P. , Chauvel, P. , & Liégeois‐Chauvel, C. (2008). Spatio temporal dynamics of face recognition. Cerebral Cortex, 18, 997–1009. 10.1093/cercor/bhm140 PubMed DOI

Barnett, L. , & Seth, A. K. (2014). The MVGC multivariate granger causality toolbox: A new approach to granger causal inference. Journal of Neuroscience Methods, 223, 50–68. 10.1016/j.jneumeth.2013.10.018 PubMed DOI

Barragan‐Jason, G. , Cauchoix, M. , & Barbeau, E. (2015). The neural speed of familiar face recognition. Neuropsychologia, 75, 390–401. 10.1016/j.neuropsychologia.2015.06.017 PubMed DOI

Basile, B. M. , Templer, V. L. , Gazes, R. P. , & Hampton, R. R. (2020). Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions. Science Advances, 6(29), eaaz0484. 10.1126/sciadv.aaz0484 PubMed DOI PMC

Bassett, D. S. , Wymbs, N. F. , Porter, M. A. , Mucha, P. J. , Carlson, J. M. , & Grafton, S. T. (2011). Dynamic reconfiguration of human brain networks during learning. Proceedings of the National Academy of Sciences, 108, 7641–7646. 10.1073/pnas.1018985108 PubMed DOI PMC

Bastin, C. , Besson, G. , Simon, J. , Delhaye, E. , Geurten, M. , Willems, S. , & Salmon, E. (2019). An integrative memory model of recollection and familiarity to understand memory deficits. Behavioral and Brain Sciences, 42, e281. 10.1017/S0140525X19000621 PubMed DOI

Benjamini, Y. , & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57(1), 289–300. 10.1111/j.2517-6161.1995.tb02031 DOI

Besson, G. , Ceccaldi, M. , Didic, M. , & Barbeau, E. J. (2012). The speed of visual recognition memory. Visual Cognition, 20, 1131–1152. 10.1080/13506285.2012.724034 DOI

Brady, T. F. , Konkle, T. , Alvarez, G. A. , & Oliva, A. (2008). Visual long‐term memory has a massive storage capacity for object details. Proceedings of the National Academy of Sciences, 105, 14325–14329. 10.1073/pnas.0803390105 PubMed DOI PMC

Braun, U. , Schäfer, A. , Walter, H. , Erk, S. , Romanczuk‐Seiferth, N. , Haddad, L. , Schweiger, J. I. , Grimm, O. , Heinz, A. , Tost, H. , Meyer‐Lindenberg, A. , & Bassett, D. S. (2015). Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proceedings of the National Academy of Sciences, 112, 11678–11683. 10.1073/pnas.1422487112 PubMed DOI PMC

Brown, M. W. , & Aggleton, J. P. (2001). Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nature Reviews Neuroscience, 2, 51–61. 10.1038/35049064 PubMed DOI

Burke, J. F. , Long, N. M. , Zaghloul, K. A. , Sharan, A. D. , Sperling, M. R. , & Kahana, M. J. (2014). Human intracranial high‐frequency activity maps episodic memory formation in space and time. NeuroImage, 85, 834–843. 10.1016/j.neuroimage.2013.06.067 PubMed DOI PMC

Calhoun, V. D. , Miller, R. , Pearlson, G. , & Adali, T. (2014). The chronnectome: Time‐varying connectivity networks as the next frontier in fMRI data discovery. Neuron, 84(2), 262–274. 10.1016/j.neuron.2014.10.015 PubMed DOI PMC

Cohen, J. R. , & D'Esposito, M. (2016). The segregation and integration of distinct brain networks and their relationship to cognition. The Journal of Neuroscience, 36, 12083–12094. 10.1523/jneurosci.2965-15.2016 PubMed DOI PMC

Deco, G. , Tononi, G. , Boly, M. , & Kringelbach, M. L. (2015). Rethinking segregation and integration: Contributions of whole‐brain modelling. Nature Reviews Neuroscience, 16, 430–439. 10.1038/nrn3963 PubMed DOI

Despouy, E. , Curot, J. , Deudon, M. , Gardy, L. , Denuelle, M. , Sol, J.‐C. , Lotterie, J.‐A. , Valton, L. , & Barbeau, E. J. (2020). A fast visual recognition memory system in humans identified using intracerebral ERP. Cerebral Cortex, 30, 2961–2971. 10.1093/cercor/bhz287 PubMed DOI

DiCarlo, J. , Zoccolan, D. , & Rust, N. (2012). How does the brain solve visual object recognition? Neuron, 73, 415–434. 10.1016/j.neuron.2012.01.010 PubMed DOI PMC

Efron, B. , & Tibshirani, R. J. (1994). An introduction to the bootstrap. CRC Press.

Eichenbaum, H. , Yonelinas, A. P. , & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152. 10.1146/annurev.neuro.30.051606.094328 PubMed DOI PMC

Eickhoff, S. B. , Stephan, K. E. , Mohlberg, H. , Grefkes, C. , Fink, G. R. , Amunts, K. , & Zilles, K. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25, 1325–1335. 10.1016/j.neuroimage.2004.12.034 PubMed DOI

Ekman, M. , Derrfuss, J. , Tittgemeyer, M. , & Fiebach, C. J. (2012). Predicting errors from reconfiguration patterns in human brain networks. Proceedings of the National Academy of Sciences, 109, 16714–16719. 10.1073/pnas.1207523109 PubMed DOI PMC

Elger, C. E. , Grunwald, T. , Lehnertz, K. , Kutas, M. , Helmstaedter, C. , Brockhaus, A. , van Roost, D. , & Heinze, H. J. (1997). Human temporal lobe potentials in verbal learning and memory processes. Neuropsychologia, 35, 657–667. 10.1016/s0028-3932(96)00110-8 PubMed DOI

Gaillard, R. , Dehaene, S. , Adam, C. , Clémenceau, S. , Hasboun, D. , Baulac, M. , Cohen, L. , & Naccache, L. (2009). Converging intracranial markers of conscious access. PLoS Biology, 7(3), e1000061. 10.1371/journal.pbio.1000061 PubMed DOI PMC

Goddard, E. , Carlson, T. A. , Dermody, N. , & Woolgar, A. (2016). Representational dynamics of object recognition: Feedforward and feedback information flows. NeuroImage, 128, 385–397. 10.1016/j.neuroimage.2016.01.006 PubMed DOI

Gonzalez, A. , Hutchinson, J. B. , Uncapher, M. R. , Chen, J. , LaRocque, K. F. , Foster, B. L. , Rangarajan, V. , Parvizi, J. , & Wagner, A. D. (2015). Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions. Proceedings of the National Academy of Sciences, 112, 11066–11071. 10.1073/pnas.1510749112 PubMed DOI PMC

Guerin, S. A. , & Miller, M. B. (2009). Lateralization of the parietal old/new effect: An event‐related fMRI study comparing recognition memory for words and faces. NeuroImage, 44(1), 232–242. 10.1016/j.neuroimage.2008.08.035 PubMed DOI

Hill, P. F. , King, D. R. , Lega, B. C. , & Rugg, M. D. (2020). Comparison of fMRI correlates of successful episodic memory encoding in temporal lobe epilepsy patients and healthy controls. NeuroImage, 207, 116397. 10.1016/j.neuroimage.2019.116397 PubMed DOI PMC

Hindriks, R. , Adhikari, M. H. , Murayama, Y. , Ganzetti, M. , Mantini, D. , Logothetis, N. K. , & Deco, G. (2016). Can sliding‐window correlations reveal dynamic functional connectivity in resting‐state fMRI? NeuroImage, 127, 242–256. 10.1016/j.neuroimage.2015.11.055 PubMed DOI PMC

Hlinka, J. , & Hadrava, M. (2015). On the danger of detecting network states in white noise. Frontiers in Computational Neuroscience, 9, 11. 10.3389/fncom.2015.00011 PubMed DOI PMC

Hoppstädter, M. , Baeuchl, C. , Diener, C. , Flor, H. , & Meyer, P. (2015). Simultaneous EEG–fMRI reveals brain networks underlying recognition memory ERP old/new effects. NeuroImage, 116, 112–122. 10.1016/j.neuroimage.2015.05.026 PubMed DOI

Hutchison, R. M. , Womelsdorf, T. , Allen, E. A. , Bandettini, P. A. , Calhoun, V. D. , Corbetta, M. , Della Penna, S. , Duyn, J. H. , Glover, G. H. , Gonzalez‐Castillo, J. , Handwerker, D. A. , Keilholz, S. , Kiviniemi, V. , Leopold, D. A. , de Pasquale, F. , Sporns, O. , Walter, M. , & Chang, C. (2013). Dynamic functional connectivity: Promise, issues, and interpretations. NeuroImage, 80, 360–378. 10.1016/j.neuroimage.2013.05.079 PubMed DOI PMC

Ishai, A. , Bikle, P. C. , & Ungerleider, L. G. (2006). Temporal dynamics of face repetition suppression. Brain Research Bulletin, 70, 289–295. 10.1016/j.brainresbull.2006.06.002 PubMed DOI

Kitzbichler, M. G. , Henson, R. N. A. , Smith, M. L. , Nathan, P. J. , & Bullmore, E. T. (2011). Cognitive effort drives workspace configuration of human brain functional networks. Journal of Neuroscience, 31, 8259–8270. 10.1523/jneurosci.0440-11.2011 PubMed DOI PMC

Krzywinski, M. , Schein, J. , Birol, I. , Connors, J. , Gascoyne, R. , Horsman, D. , Jones, S. J. , & Marra, M. A. (2009). Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645. 10.1101/gr.092759.109 PubMed DOI PMC

Lachaux, J. P. , Rudrauf, D. , & Kahane, P. (2003). Intracranial EEG and human brain mapping. Journal of Physiology, Paris, 97, 613–628. 10.1016/j.jphysparis.2004.01.018 PubMed DOI

Lahiri, S. N. (2003). Resampling methods for dependent data. Springer series in statistics. Springer‐Verlag. 10.1007/978-1-4757-3803-2 DOI

Larzabal, C. , Tramoni, E. , Muratot, S. , Thorpe, S. J. , & Barbeau, E. J. (2018). Extremely long‐term memory and familiarity after 12 years. Cognition, 170, 254–262. 10.1016/j.cognition.2017.10.009 PubMed DOI PMC

Latora, V. , & Marchiori, M. (2001). Efficient behavior of small‐world networks. Physical Review Letters, 87, 198701. 10.1103/PhysRevLett.87.198701 PubMed DOI

Maffei, A. , & Sessa, P. (2021). Time‐resolved connectivity reveals the “how” and “when” of brain networks reconfiguration during face processing. Neuroimage: Reports, 1(2), 100022. 10.1016/j.ynirp.2021.100022 DOI

Maillard, L. , Barbeau, E. J. , Baumann, C. , Koessler, L. , Bénar, C. , Chauvel, P. , & Liégeois‐Chauvel, C. (2011). From perception to recognition memory: Time course and lateralization of neural substrates of word and abstract picture processing. Journal of Cognitive Neuroscience, 23, 782–800. 10.1162/jocn.2010.21434 PubMed DOI

Mashour, G. A. , Roelfsema, P. , Changeux, J.‐P. , & Dehaene, S. (2020). Conscious processing and the global neuronal workspace hypothesis. Neuron, 105(5), 776–798. 10.1016/j.neuron.2020.01.026 PubMed DOI PMC

Meunier, D. , Fonlupt, P. , Saive, A.‐L. , Plailly, J. , Ravel, N. , & Royet, J.‐P. (2014). Modular structure of functional networks in olfactory memory. NeuroImage, 95, 264–275. 10.1016/j.neuroimage.2014.03.041 PubMed DOI

Milner, B. (1972). Disorders of learning and memory after temporal lobe lesions in man. Neurosurgery, 19, 421–446. 10.1093/neurosurgery/19.CNsuppl1.421 PubMed DOI

Newman, M. E. J. (2006). Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America, 103, 8577–8582. 10.1073/pnas.0601602103 PubMed DOI PMC

Patterson, K. , & Bradshaw, J. L. (1975). Differential hemispheric mediation of nonverbal visual stimuli. Journal of Experimental Psychology: Human Perception and Performance, 1, 246–252. 10.1037//0096-1523.1.3.246 PubMed DOI

Penn, A. (2020). iboot: Iterated bootstrap for small samples and samples with complex dependence structures. https://github.com/acp29/iboot 10.5281/ZENODO.3992393 DOI

Petrovska, J. , Loos, E. , Coynel, D. , Egli, T. , Papassotiropoulos, A. , de Quervain, D. J. , & Milnik, A. (2021). Recognition memory performance can be estimated based on brain activation networks. Behavioural Brain Research, 408, 113285. 10.1016/j.bbr.2021.113285 PubMed DOI

Pidnebesna, A. , Sanda, P. , Kalina, A. , Hammer, J. , Marusic, P. , Vlcek, K. , & Hlinka, J. (2022). Tackling the challenges of group network inference from intracranial EEG data. Frontiers in Neuroscience, 16, 1061867. 10.3389/fnins.2022.1061867 PubMed DOI PMC

Politis, D. N. , & White, H. (2004). Automatic block‐length selection for the dependent bootstrap. Econometric Reviews, 23, 53–70. 10.1081/ETC-120028836 DOI

Preti, M. G. , Bolton, T. A. , & Van De Ville, D. (2017). The dynamic functional connectome: State‐of‐the‐art and perspectives. NeuroImage, 160, 41–54. 10.1016/j.neuroimage.2016.12.061 PubMed DOI

Rijsbergen, N. J. V. , & Schyns, P. G. (2009). Dynamics of trimming the content of face representations for categorization in the brain. PLoS Computational Biology, 5, e1000561. 10.1371/journal.pcbi.1000561 PubMed DOI PMC

Rousselet, G. A. , Thorpe, S. J. , & Fabre‐Thorpe, M. (2004). Processing of one, two or four natural scenes in humans: The limits of parallelism. Vision Research, 44(9), 877–894. 10.1016/j.visres.2003.11.014 PubMed DOI

Rubinov, M. , & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52, 1059–1069. 10.1016/j.neuroimage.2009.10.003 PubMed DOI

Schreiber, T. , & Schmitz, A. (2000). Surrogate time series. Physica D: Nonlinear Phenomena, 142, 346–382. 10.1016/S0167-2789(00)00043-9 DOI

Seth, A. K. , Barrett, A. B. , & Barnett, L. (2015). Granger causality analysis in neuroscience and neuroimaging. Journal of Neuroscience, 35, 3293–3297. 10.1523/jneurosci.4399-14.2015 PubMed DOI PMC

Shine, J. M. , Bissett, P. G. , Bell, P. T. , Koyejo, O. , Balsters, J. H. , Gorgolewski, K. J. , Moodie, C. A. , & Poldrack, R. A. (2016). The dynamics of functional brain networks: Integrated network states during cognitive task performance. Neuron, 92, 544–554. 10.1016/j.neuron.2016.09.018 PubMed DOI PMC

Sporns, O. (2007). Brain connectivity. Scholarpedia, 2, 4695. 10.4249/scholarpedia.4695 DOI

Sporns, O. (2011). The non‐random brain: Efficiency, economy, and complex dynamics. Frontiers in Computational Neuroscience, 5, 5. 10.3389/fncom.2011.00005 PubMed DOI PMC

Sporns, O. (2013). Network attributes for segregation and integration in the human brain. Current Opinion in Neurobiology, 23, 162–171. 10.1016/j.conb.2012.11.015 PubMed DOI

Sporns, O. , & Betzel, R. F. (2016). Modular brain networks. Annual Review of Psychology, 67, 613–640. 10.1146/annurev-psych-122414-033634 PubMed DOI PMC

Staresina, B. P. , Fell, J. , Do Lam, A. T. A. , Axmacher, N. , & Henson, R. N. (2012). Memory signals are temporally dissociated in and across human hippocampus and perirhinal cortex. Nature Neuroscience, 15, 1167–1173. 10.1038/nn.3154 PubMed DOI PMC

Staresina, B. P. , & Wimber, M. (2019). A neural chronometry of memory recall. Trends in Cognitive Sciences, 23(12), 1071–1085. 10.1016/j.tics.2019.09.011 PubMed DOI

Tzourio‐Mazoyer, N. , Landeau, B. , Papathanassiou, D. , Crivello, F. , Etard, O. , Delcroix, N. , Mazoyer, B. , & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single‐subject brain. NeuroImage, 15, 273–289. 10.1006/nimg.2001.0978 PubMed DOI

VanRullen, R. , & Thorpe, S. J. (2001). Is it a bird? Is it a plane? Ultra‐rapid visual categorisation of natural and artifactual objects. Perception, 30(6), 655–668. 10.1068/p3029 PubMed DOI

Varela, F. , Lachaux, J.‐P. , Rodriguez, E. , & Martinerie, J. (2001). The brainweb: Phase synchronization and largescale integration. Nature Reviews Neuroscience, 2, 229–239. 10.1038/35067550 PubMed DOI

Westphal, A. J. , Wang, S. , & Rissman, J. (2017). Episodic memory retrieval benefits from a less modular brain network organization. Journal of Neuroscience, 37, 3523–3531. 10.1523/jneurosci.2509-16.2017 PubMed DOI PMC