Processing of memory is supported by coordinated activity in a network of sensory, association, and motor brain regions. It remains a major challenge to determine where memory is encoded for later retrieval. Here, we used direct intracranial brain recordings from epilepsy patients performing free recall tasks to determine the temporal pattern and anatomical distribution of verbal memory encoding across the entire human cortex. High γ frequency activity (65-115 Hz) showed consistent power responses during encoding of subsequently recalled and forgotten words on a subset of electrodes localized in 16 distinct cortical areas activated in the tasks. More of the high γ power during word encoding, and less power before and after the word presentation, was characteristic of successful recall and observed across multiple brain regions. Latencies of the induced power changes and this subsequent memory effect (SME) between the recalled and forgotten words followed an anatomical sequence from visual to prefrontal cortical areas. Finally, the magnitude of the memory effect was unexpectedly found to be the largest in selected brain regions both at the top and at the bottom of the processing stream. These included the language processing areas of the prefrontal cortex and the early visual areas at the junction of the occipital and temporal lobes. Our results provide evidence for distributed encoding of verbal memory organized along a hierarchical posterior-to-anterior processing stream.

Department of Electrical and Computer Engineering University of Illinois Urbana Champaign IL 61801

Department of Neurology Dartmouth Hitchcock Medical Center Lebanon NH 03756

Department of Neurology Mayo Clinic Rochester MN 55905

Department of Neurology Thomas Jefferson University Hospital Philadelphia PA 19107

Department of Neurology University of Pennsylvania Hospital Philadelphia PA 19104

Department of Neurosurgery Baylor College of Medicine Houston TX 77030

Department of Neurosurgery Emory University Atlanta GA 30322

Department of Neurosurgery UT Southwestern Medical Center Dallas TX 75390

Department of Physiology and Biomedical Engineering Mayo Clinic Rochester MN 55905

Department of Psychology University of Pennsylvania Philadelphia PA 19104

Institute of Informatics Robotics and Cybernetics Czech Technical University Prague Czech Republic 16000

Multimedia Systems Department Gdansk University of Technology Faculty of Electronics Telecommunications and Informatics Gdansk Poland 80233

Zobrazit více v PubMed

Binder JR, Desai RH (2011) The neurobiology of semantic memory. Trends Cogn Sci 15:527–536. 10.1016/j.tics.2011.10.001 PubMed DOI PMC

Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19:2767–2796. 10.1093/cercor/bhp055 PubMed DOI PMC

Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: a platform for analyzing neural signals. J Neurosci Methods 192:146–151. 10.1016/j.jneumeth.2010.06.020 PubMed DOI PMC

Burke JF, Long NM, Zaghloul KA, Sharan AD, Sperling MR, Kahana MJ (2014) Human intracranial high-frequency activity maps episodic memory formation in space and time. Neuroimage 85[Pt 2]:834–843. 10.1016/j.neuroimage.2013.06.067 PubMed DOI PMC

Bussey TJ, Saksida LM (2007) Memory, perception, and the ventral visual-perirhinal-hippocampal stream: thinking outside of the boxes. Hippocampus 17:898–908. 10.1002/hipo.20320 PubMed DOI

Canolty RT, Soltani M, Dalal SS, Edwards E, Dronkers NF, Nagarajan SS, Kirsch HE, Barbaro NM, Knight RT (2007) Spatiotemporal dynamics of word processing in the human brain. Front Neurosci 1:185–196. 10.3389/neuro.01.1.1.014.2007 PubMed DOI PMC

Collard MJ, Fifer MS, Benz HL, McMullen DP, Wang Y, Milsap GW, Korzeniewska A, Crone NE (2016) Cortical subnetwork dynamics during human language tasks. Neuroimage 135:261–272. 10.1016/j.neuroimage.2016.03.072 PubMed DOI PMC

Crone NE, Sinai A, Korzeniewska A (2006) High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res 159:275–295. 10.1016/S0079-6123(06)59019-3 PubMed DOI

Dalal SS, Baillet S, Adam C, Ducorps A, Schwartz D, Jerbi K, Bertrand O, Garnero L, Martinerie J, Lachaux J-P (2009) Simultaneous MEG and intracranial EEG recordings during attentive reading. Neuroimage 45:1289–1304. 10.1016/j.neuroimage.2009.01.017 PubMed DOI

Desimone R, Ungerleider LG (1989) Neural mechanisms of visual processing in monkeys In: Handbook of neuropsychology, pp 267–299. New York: Elsevier Science.

Dotson NM, Hoffman SJ, Goodell B, Gray CM (2018) Feature-based visual short-term memory is widely distributed and hierarchically organized. Neuron 99:215–226. 10.1016/j.neuron.2018.05.026 PubMed DOI PMC

Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50. 10.1038/35036213 PubMed DOI

Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF, Knight RT, Crone NE (2015) Redefining the role of Broca’s area in speech. Proc Natl Acad Sci USA 112:2871–2875. 10.1073/pnas.1414491112 PubMed DOI PMC

Gaffan D (2002) Against memory systems. Philos Trans R Soc B Biol Sci 357:1111–1121. 10.1098/rstb.2002.1110 PubMed DOI PMC

Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154. 10.1113/jphysiol.1962.sp006837 PubMed DOI PMC

Huth AG, de Heer WA, Griffiths TL, Theunissen FE, Gallant JL (2016) Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532:453–458. 10.1038/nature17637 PubMed DOI PMC

Jerbi K, Ossandón T, Hamamé CM, Senova S, Dalal SS, Jung J, Minotti L, Bertrand O, Berthoz A, Kahane P, Lachaux J-P (2009) Task-related gamma-band dynamics from an intracerebral perspective: review and implications for surface EEG and MEG. Hum Brain Mapp 30:1758–1771. 10.1002/hbm.20750 PubMed DOI PMC

Johnson EL, Knight RT (2015) Intracranial recordings and human memory. Curr Opin Neurobiol 31:18–25. 10.1016/j.conb.2014.07.021 PubMed DOI PMC

Kahana M (2012) Foundations of human memory. Oxford, New York: Oxford University Press.

Kim H (2011) Neural activity that predicts subsequent memory and forgetting: a meta-analysis of 74 fMRI studies. Neuroimage 54:2446–2461. 10.1016/j.neuroimage.2010.09.045 PubMed DOI

Knight RT (2007) Neural networks debunk phrenology. Science 316:1578–1579. 10.1126/science.1144677 PubMed DOI

Kucewicz MT, Cimbalnik J, Matsumoto JY, Brinkmann BH, Bower MR, Vasoli V, Sulc V, Meyer F, Marsh WR, Stead SM, Worrell GA (2014) High frequency oscillations are associated with cognitive processing in human recognition memory. Brain 137:2231–2244. 10.1093/brain/awu149 PubMed DOI PMC

Kucewicz MT, Berry BM, Kremen V, Brinkmann BH, Sperling MR, Jobst BC, Gross RE, Lega B, Sheth SA, Stein JM, Das SR, Gorniak R, Stead SM, Rizzuto DS, Kahana MJ, Worrell GA (2017) Dissecting gamma frequency activity during human memory processing. Brain 140:1337–1350. 10.1093/brain/awx043 PubMed DOI

Kucewicz MT, Berry BM, Miller LR, Khadjevand F, Ezzyat Y, Stein JM, Kremen V, Brinkmann BH, Wanda P, Sperling MR, Gorniak R, Davis KA, Jobst BC, Gross RE, Lega B, Van Gompel J, Stead SM, Rizzuto DS, Kahana MJ, Worrell GA (2018a) Evidence for verbal memory enhancement with electrical brain stimulation in the lateral temporal cortex. Brain 141:971–978. 10.1093/brain/awx373 PubMed DOI

Kucewicz MT, Berry BM, Kremen V, Miller LR, Khadjevand F, Ezzyat Y, Stein JM, Wanda P, Sperling MR, Gorniak R, Davis KA, Jobst BC, Gross RE, Lega B, Stead SM, Rizzuto DS, Kahana MJ, Worrell GA (2018b) Electrical stimulation modulates high γ activity and human memory performance. eNeuro 5: ENEURO.0369-17.2018. 10.1523/ENEURO.0369-17.2018 PubMed DOI PMC

Lachaux JP, Axmacher N, Mormann F, Halgren E, Crone NE (2012) High-frequency neural activity and human cognition: past, present and possible future of intracranial EEG research. Prog Neurobiol 98:279–301. 10.1016/j.pneurobio.2012.06.008 PubMed DOI PMC

Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157. 10.1038/35084005 PubMed DOI

Long NM, Burke JF, Kahana MJ (2014) Subsequent memory effect in intracranial and scalp EEG. Neuroimage 84:488–494. 10.1016/j.neuroimage.2013.08.052 PubMed DOI PMC

Mano QR, Humphries C, Desai RH, Seidenberg MS, Osmon DC, Stengel BC, Binder JR (2013) The role of left occipitotemporal cortex in reading: reconciling stimulus, task, and lexicality effects. Cereb Cortex 23:988–1001. 10.1093/cercor/bhs093 PubMed DOI PMC

Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613. 10.1002/ana.410280502 PubMed DOI

Milner D, Goodale M (2006) The visual brain in action, Ed 2 Oxford, New York: Oxford University Press.

Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RAW (2005) Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948–951. 10.1126/science.1110948 PubMed DOI

Rich EL, Wallis JD (2017) Spatiotemporal dynamics of information encoding revealed in orbitofrontal high-gamma. Nat Commun 8:1139. 10.1038/s41467-017-01253-5 PubMed DOI PMC

Riès SK, Dhillon RK, Clarke A, King-Stephens D, Laxer KD, Weber PB, Kuperman RA, Auguste KI, Brunner P, Schalk G, Lin JJ, Parvizi J, Crone NE, Dronkers NF, Knight RT (2017) Spatiotemporal dynamics of word retrieval in speech production revealed by cortical high-frequency band activity. Proc Natl Acad Sci USA 114:E4530–E4538. 10.1073/pnas.1620669114 PubMed DOI PMC

Riesenhuber M, Poggio T (1999) Hierarchical models of object recognition in cortex. Nat Neurosci 2:1019–1025. 10.1038/14819 PubMed DOI

Rissman J, Wagner AD (2012) Distributed representations in memory: insights from functional brain imaging. Annu Rev Psychol 63:101–128. 10.1146/annurev-psych-120710-100344 PubMed DOI PMC

Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, Tully MS, Kahana MJ (2007) Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17:1190–1196. 10.1093/cercor/bhl030 PubMed DOI

Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121–134. 10.1038/nrn3137 PubMed DOI

Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349–374. 10.1146/annurev.ph.55.030193.002025 PubMed DOI

Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380–1386. 10.1126/science.1896849 PubMed DOI

Ungerleider LG, Mishkin M (1982) Two cortical visual systems In: Analysis of visual behavior, pp 549–586. Cambridge, MA: MIT Press.

Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229–239. 10.1038/35067550 PubMed DOI

Vidal JR, Freyermuth S, Jerbi K, Hamamé CM, Ossandon T, Bertrand O, Minotti L, Kahane P, Berthoz A, Lachaux J-P (2012) Long-distance amplitude correlations in the high γ band reveal segregation and integration within the reading network. J Neurosci 32:6421–6434. 10.1523/JNEUROSCI.4363-11.2012 PubMed DOI PMC

Wang X, Wu W, Ling Z, Xu Y, Fang Y, Wang X, Binder JR, Men W, Gao JH, Bi Y (2018) Organizational principles of abstract words in the human brain. Cereb Cortex 28:4305–4318. 10.1093/cercor/bhx283 PubMed DOI

Wang Y, Fifer MS, Flinker A, Korzeniewska A, Cervenka MC, Anderson WS, Boatman-Reich DF, Crone NE (2016) Spatial-temporal functional mapping of language at the bedside with electrocorticography. Neurology 86:1181–1189. 10.1212/WNL.0000000000002525 PubMed DOI PMC

Watson BO, Ding M, Buzsaki G (2017) Temporal coupling of field potentials and action potentials in the neocortex. Eur J Neurosci 48:2482–2497. 10.1111/ejn.13807 PubMed DOI PMC

Wurtz RH (2009) Recounting the impact of Hubel and Wiesel. J Physiol 587:2817–2823. 10.1113/jphysiol.2009.170209 PubMed DOI PMC

High frequency oscillations in human memory and cognition: a neurophysiological substrate of engrams?

Hotspot of human verbal memory encoding in the left anterior prefrontal cortex

Intracranial electrophysiological recordings from the human brain during memory tasks with pupillometry

Leveraging electrophysiologic correlates of word encoding to map seizure onset zone in focal epilepsy: Task-dependent changes in epileptiform activity, spectral features, and functional connectivity

Unsupervised machine-learning classification of electrophysiologically active electrodes during human cognitive task performance