The way the human brain represents speech in memory is still unknown. An obvious characteristic of speech is its evolvement over time. During speech processing, neural oscillations are modulated by the temporal properties of the acoustic speech signal, but also acquired knowledge on the temporal structure of language influences speech perception-related brain activity. This suggests that speech could be represented in the temporal domain, a form of representation that the brain also uses to encode autobiographic memories. Empirical evidence for such a memory code is lacking. We investigated the nature of speech memory representations using direct cortical recordings in the left perisylvian cortex during delayed sentence reproduction in female and male patients undergoing awake tumor surgery. Our results reveal that the brain endogenously represents speech in the temporal domain. Temporal pattern similarity analyses revealed that the phase of frontotemporal low-frequency oscillations, primarily in the beta range, represents sentence identity in working memory. The positive relationship between beta power during working memory and task performance suggests that working memory representations benefit from increased phase separation.SIGNIFICANCE STATEMENT Memory is an endogenous source of information based on experience. While neural oscillations encode autobiographic memories in the temporal domain, little is known on their contribution to memory representations of human speech. Our electrocortical recordings in participants who maintain sentences in memory identify the phase of left frontotemporal beta oscillations as the most prominent information carrier of sentence identity. These observations provide evidence for a theoretical model on speech memory representations and explain why interfering with beta oscillations in the left inferior frontal cortex diminishes verbal working memory capacity. The lack of sentence identity coding at the syllabic rate suggests that sentences are represented in memory in a more abstract form compared with speech coding during speech perception and production.

Department of Neurology Christian Albrechts University 24105 Kiel Germany

Department of Neurology Goethe University 60528 Frankfurt Germany

Department of Neurology Palacky University and University Hospital Olomouc 77147 Olomouc Czech Republic

Department of Neurosurgery Goethe University 60528 Frankfurt Germany

Institute for Cell Biology and Neuroscience Goethe University 60438 Frankfurt Germany

Max Planck Institute for Empirical Aesthetics 60322 Frankfurt Germany

Radboud University Donders Institute for Brain Cognition and Behaviour 6525 HR Nijmegen The Netherlands and

School of Psychology at University of Birmingham B15 2TT Birmingham United Kingdom

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Alderson-Day B, Fernyhough C (2015) Inner speech: development, cognitive functions, phenomenology, and neurobiology. Psychol Bull 141:931–965. 10.1037/bul0000021 PubMed DOI PMC

Arnal LH. (2012) Predicting “when” using the motor system's beta-band oscillations. Front Hum Neurosci 6:225. 10.3389/fnhum.2012.00225 PubMed DOI PMC

Ashburner J. (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113. 10.1016/j.neuroimage.2007.07.007 PubMed DOI

Baddeley A. (2003) Working memory and language: an overview. J Commun Dis 36:189–208. 10.1016/S0021-9924(03)00019-4 PubMed DOI

Bastiaansen M, Magyari L, Hagoort P (2010) Syntactic unification operations are reflected in oscillatory dynamics during on-line sentence comprehension. J Cogn Neurosci 22:1333–1347. 10.1162/jocn.2009.21283 PubMed DOI

Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76:695–711. 10.1016/j.neuron.2012.10.038 PubMed DOI PMC

Behroozmand R, Ibrahim N, Korzyukov O, Robin DA, Larson CR (2015) Functional role of delta and theta band oscillations for auditory feedback processing during vocal pitch motor control. Front Neurosci 9:109. 10.3389/fnins.2015.00109 PubMed DOI PMC

Bonhage CE, Fiebach CJ, Bahlmann J, Mueller JL (2014) Brain signature of working memory for sentence structure: enriched encoding and facilitated maintenance. J Cogn Neurosci 26:1654–1671. 10.1162/jocn_a_00566 PubMed DOI

Bonhage CE, Meyer L, Gruber T, Friederici AD, Mueller JL (2017) Oscillatory EEG dynamics underlying automatic chunking during sentence processing. Neuroimage 152:647–657. 10.1016/j.neuroimage.2017.03.018 PubMed DOI

Bouchard KE, Mesgarani N, Johnson K, Chang EF (2013) Functional organization of human sensorimotor cortex for speech articulation. Nature 495:327–332. 10.1038/nature11911 PubMed DOI PMC

Bouton S, Chambon V, Tyrand R, Guggisberg AG, Seeck M, Karkar S, van de Ville D, Giraud AL (2018) Focal versus distributed temporal cortex activity for speech sound category assignment. Proc Natl Acad Sci U S A 115:E1299–E1308. 10.1073/pnas.1714279115 PubMed DOI PMC

Bressler SL, Richter CG (2015) Interareal oscillatory synchronization in top-down neocortical processing. Curr Opin Neurobiol 31:62–66. 10.1016/j.conb.2014.08.010 PubMed DOI

Buchsbaum BR, D'Esposito M (2008) The search for the phonological store: from loop to convolution. J Cogn Neurosci 20:762–778. 10.1162/jocn.2008.20501 PubMed DOI

Busch RM, Love TE, Jehi LE, Ferguson L, Yardi R, Najm I, Bingaman W, Gonzalez-Martinez J (2015) Effect of invasive EEG monitoring on cognitive outcome after left temporal lobe epilepsy surgery. Neurology 85:1475–1481. 10.1212/WNL.0000000000002066 PubMed DOI PMC

Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860–1862. 10.1126/science.1138071 PubMed DOI

Buzsáki G. (2006) Rhythms of the brain. Oxford: Oxford UP.

Cheung C, Hamiton LS, Johnson K, Chang EF (2016) The auditory representation of speech sounds in human motor cortex. eLife 5:133. 10.7554/eLife.12577 PubMed DOI PMC

Cogan GB, Thesen T, Carlson C, Doyle W, Devinsky O, Pesaran B (2014) Sensory-motor transformations for speech occur bilaterally. Nature 507:94–98. 10.1038/nature12935 PubMed DOI PMC

Cogan GB, Iyer A, Melloni L, Thesen T, Friedman D, Doyle W, Devinsky O, Pesaran B (2017) Manipulating stored phonological input during verbal working memory. Nat Neurosci 20:279–286. 10.1038/nn.4459 PubMed DOI PMC

Courtemanche R, Fujii N, Graybiel AM (2003) Synchronous, focally modulated β-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J Neurosci 23:11741–11752. 10.1523/JNEUROSCI.23-37-11741.2003 PubMed DOI PMC

Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage 9:179–194. 10.1006/nimg.1998.0395 PubMed DOI

Ding N, Simon JZ (2014) Cortical entrainment to continuous speech: functional roles and interpretations. Front Hum Neurosci 8:311. 10.3389/fnhum.2014.00311 PubMed DOI PMC

Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20:143–149. 10.1016/j.conb.2010.01.004 PubMed DOI

Flinker A, Chang EF, Kirsch HE, Barbaro NM, Crone NE, Knight RT (2010) Single-trial speech suppression of auditory cortex activity in humans. J Neurosci 30:16643–16650. 10.1523/JNEUROSCI.1809-10.2010 PubMed DOI PMC

Fujioka T, Trainor LJ, Large EW, Ross B (2012) Internalized timing of isochronous sounds is represented in neuromagnetic beta oscillations. J Neurosci 32:1791–1802. 10.1523/JNEUROSCI.4107-11.2012 PubMed DOI PMC

Ghitza O. (2011) Linking speech perception and neurophysiology: speech decoding guided by cascaded oscillators locked to the input rhythm. Front Psychol 2:130. 10.3389/fpsyg.2011.00130 PubMed DOI PMC

Ghitza O, Greenberg S (2009) On the possible role of brain rhythms in speech perception: intelligibility of time-compressed speech with periodic and aperiodic insertions of silence. Phonetica 66:113–126. 10.1159/000208934 PubMed DOI

Giraud AL, Poeppel D (2012) Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15:511–517. 10.1038/nn.3063 PubMed DOI PMC

Golumbic ZE, Ding N, Bickel S, Lakatos P, Schevon CA, McKhann GM, Goodman RR, Emerson R, Mehta AD, Simon JZ, Poeppel D, Schroeder CE (2013) Mechanisms underlying selective neuronal tracking of attended speech at a “cocktail party.” Neuron 77:980–991. 10.1016/j.neuron.2012.12.037 PubMed DOI PMC

Gompf F, Pflug A, Laufs H, Kell CA (2017) Non-linear relationship between BOLD activation and amplitude of beta oscillations in the supplementary motor area during rhythmic finger tapping and internal timing. Front Hum Neurosci 11:582. 10.3389/fnhum.2017.00582 PubMed DOI PMC

Grabner G, Janke AL, Budge MM, Smith D, Pruessner J, Collins DL (2006) Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. In: Medical image computing and computer-assisted intervention: MICCAI 2006 (Hutchison D, Kanade T, Kittler J, Kleinberg JM, Mattern F, Mitchell JC, Naor M, Nierstrasz O, Pandu Rangan C, Steffen B, Sudan M, Terzopoulos D, Tygar D, Vardi MY, Weikum G, Larsen R, Nielsen M, Sporring J, eds), pp 58–66. Berlin: Springer. PubMed

Gross J, Hoogenboom N, Thut G, Schyns P, Panzeri S, Belin P, Garrod S (2013) Speech rhythms and multiplexed oscillatory sensory coding in the human brain. PLoS Biol 11:e1001752. 10.1371/journal.pbio.1001752 PubMed DOI PMC

Hanslmayr S, Matuschek J, Fellner MC (2014) Entrainment of prefrontal beta oscillations induces an endogenous echo and impairs memory formation. Curr Biol 24:904–909. 10.1016/j.cub.2014.03.007 PubMed DOI

Henson RN, Eckstein D, Waszak F, Frings C, Horner AJ (2014) Stimulus-response bindings in priming. Trends Cogn Sci 18:376–384. 10.1016/j.tics.2014.03.004 PubMed DOI PMC

Herff C, Heger D, de Pesters A, Telaar D, Brunner P, Schalk G, Schultz T (2015) Brain-to-text: decoding spoken phrases from phone representations in the brain. Front Neurosci 9:217. 10.3389/fnins.2015.00217 PubMed DOI PMC

Herman AB, Houde JF, Vinogradov S, Nagarajan SS (2013) Parsing the phonological loop: activation timing in the dorsal speech stream determines accuracy in speech reproduction. J Neurosci 33:5439–5453. 10.1523/JNEUROSCI.1472-12.2013 PubMed DOI PMC

Hickok G. (2012) Computational neuroanatomy of speech production. Nat Rev Neurosci 13:135–145. 10.1038/nrn3158 PubMed DOI PMC

Hickok G, Poeppel D (2000) Towards a functional neuroanatomy of speech perception. Trends Cogn Sci 4:131–138. 10.1016/S1364-6613(00)01463-7 PubMed DOI

Hickok G, Poeppel D (2004) Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition 92:67–99. 10.1016/j.cognition.2003.10.011 PubMed DOI

Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393–402. 10.1038/nrn2113 PubMed DOI

Howe MW, Atallah HE, McCool A, Gibson DJ, Graybiel AM (2011) Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum. Proc Natl Acad Sci U S A 108:16801–16806. 10.1073/pnas.1113158108 PubMed DOI PMC

Indefrey P, Levelt WJ (2004) The spatial and temporal signatures of word production components. Cognition 92:101–144. 10.1016/j.cognition.2002.06.001 PubMed DOI

Jacquemot C, Scott SK (2006) What is the relationship between phonological short-term memory and speech processing? Trends Cogn Sci 10:480–486. 10.1016/j.tics.2006.09.002 PubMed DOI

Korzeniewska A, Franaszczuk PJ, Crainiceanu CM, Kus R, Crone NE (2011) Dynamics of large-scale cortical interactions at high gamma frequencies during word production: event related causality (ERC) analysis of human electrocorticography (ECoG). Neuroimage 56:2218–2237. 10.1016/j.neuroimage.2011.03.030 PubMed DOI PMC

Kriegeskorte N, Mur M, Bandettini P (2008) Representational similarity analysis: connecting the branches of systems neuroscience. Front Syst Neurosci 2:4. 10.3389/neuro.01.016.2008 PubMed DOI PMC

Kubanek J, Brunner P, Gunduz A, Poeppel D, Schalk G (2013) The tracking of speech envelope in the human cortex. PLoS One 8:e53398. 10.1371/journal.pone.0053398 PubMed DOI PMC

Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194–208. 10.1002/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C PubMed DOI PMC

Lam NH, Schoffelen JM, Uddén J, Hultén A, Hagoort P (2016) Neural activity during sentence processing as reflected in theta, alpha, beta, and gamma oscillations. Neuroimage 15:43–54. 10.1016/j.neuroimage.2016.03.007 PubMed DOI

Lee JH, Whittington MA, Kopell NJ (2015) Potential mechanisms underlying intercortical signal regulation via cholinergic neuromodulators. J Neurosci 35:15000–15014. 10.1523/JNEUROSCI.0629-15.2015 PubMed DOI PMC

Lotte F, Brumberg JS, Brunner P, Gunduz A, Ritaccio AL, Guan C, Schalk G (2015) Electrocorticographic representations of segmental features in continuous speech. Front Hum Neurosci 9:97. 10.3389/fnhum.2015.00097 PubMed DOI PMC

Lundqvist M, Herman P, Miller EK (2018a) Working memory. delay activity, Yes! Persistent activity? Maybe not. J Neurosci 38:7013–7019. 10.1523/JNEUROSCI.2485-17.2018 PubMed DOI PMC

Lundqvist M, Herman P, Warden MR, Brincat SL, Miller EK (2018b) Gamma and beta bursts during working memory readout suggest roles in its volitional control. Nat Commun 9:394. 10.1038/s41467-017-02791-8 PubMed DOI PMC

Luo H, Poeppel D (2007) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54:1001–1010. 10.1016/j.neuron.2007.06.004 PubMed DOI PMC

Mercier MR, Bickel S, Megevand P, Groppe DM, Schroeder CE, Mehta AD, Lado FA (2017) Evaluation of cortical local field potential diffusion in stereotactic electro-encephalography recordings: a glimpse on white matter signal. Neuroimage 147:219–232. 10.1016/j.neuroimage.2016.08.037 PubMed DOI

Mesgarani N, Chang EF (2012) Selective cortical representation of attended speaker in multi-talker speech perception. Nature 485:233–236. 10.1038/nature11020 PubMed DOI PMC

Mesgarani N, Cheung C, Johnson K, Chang EF (2014) Phonetic feature encoding in human superior temporal gyrus. Science 343:1006–1010. 10.1126/science.1245994 PubMed DOI PMC

Michalareas G, Vezoli J, van Pelt S, Schoffelen JM, Kennedy H, Fries P (2016) Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron 89:384–397. 10.1016/j.neuron.2015.12.018 PubMed DOI PMC

Michelmann S, Bowman H, Hanslmayr S (2016) The temporal signature of memories: identification of a general mechanism for dynamic memory replay in humans. PLoS Biol 14:e1002528. 10.1371/journal.pbio.1002528 PubMed DOI PMC

Miller EK, Lundqvist M, Bastos AM (2018) Working memory 2.0. Neuron 100:463–475. 10.1016/j.neuron.2018.09.023 PubMed DOI PMC

Murakami T, Kell CA, Restle J, Ugawa Y, Ziemann U (2015) Left dorsal speech stream components and their contribution to phonological processing. J Neurosci 35:1411–1422. 10.1523/JNEUROSCI.0246-14.2015 PubMed DOI PMC

Nelson MJ, El Karoui I, Giber K, Yang X, Cohen L, Koopman H, Cash SS, Naccache L, Hale JT, Pallier C, Dehaene S (2017) Neurophysiological dynamics of phrase-structure building during sentence processing. Proc Natl Acad Sci U S A 114:E3669–E3678. 10.1073/pnas.1701590114 PubMed DOI PMC

Nourski KV, Reale RA, Oya H, Kawasaki H, Kovach CK, Chen H, Howard MA 3rd, Brugge JF (2009) Temporal envelope of time-compressed speech represented in the human auditory cortex. J Neurosci 29:15564–15574. 10.1523/JNEUROSCI.3065-09.2009 PubMed DOI PMC

Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. 10.1155/2011/156869 PubMed DOI PMC

Pasley BN, David SV, Mesgarani N, Flinker A, Shamma SA, Crone NE, Knight RT, Chang EF (2012) Reconstructing speech from human auditory cortex. PLoS Biol 10:e1001251. 10.1371/journal.pbio.1001251 PubMed DOI PMC

Pei X, Leuthardt EC, Gaona CM, Brunner P, Wolpaw JR, Schalk G (2011) Spatiotemporal dynamics of electrocorticographic high gamma activity during overt and covert word repetition. Neuroimage 54:2960–2972. 10.1016/j.neuroimage.2010.10.029 PubMed DOI PMC

Peña M, Melloni L (2012) Brain oscillations during spoken sentence processing. J Cogn Neurosci 24:1149–1164. 10.1162/jocn_a_00144 PubMed DOI

Perrone-Bertolotti M, Rapin L, Lachaux JP, Baciu M, Loevenbruck H (2014) What is that little voice inside my head? Inner speech phenomenology, its role in cognitive performance, and its relation to self-monitoring. Behav Brain Res 261:220–239. 10.1016/j.bbr.2013.12.034 PubMed DOI

Potter MC, Lombardi L (1990) Regeneration in the short-term recall of sentences. J Mem Lang 29:633 10.1016/0749-596X(90)90042-X DOI

Potter MC, Lombardi L (1998) Syntactic priming in immediate recall of sentences. J Mem Lang 38:265–282. 10.1006/jmla.1997.2546 DOI

Rimmele JM, Zion Golumbic E, Schröger E, Poeppel D (2015) The effects of selective attention and speech acoustics on neural speech-tracking in a multi-talker scene. Cortex 68:144–154. 10.1016/j.cortex.2014.12.014 PubMed DOI PMC

Roelfsema PR, Engel AK, König P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157–161. 10.1038/385157a0 PubMed DOI

Salazar RF, Dotson NM, Bressler SL, Gray CM (2012) Content-specific fronto-parietal synchronization during visual working memory. Science 338:1097–1100. 10.1126/science.1224000 PubMed DOI PMC

Siegel M, Warden MR, Miller EK (2009) Phase-dependent neuronal coding of objects in short-term memory. Proc Natl Acad Sci U S A 106:21341–21346. 10.1073/pnas.0908193106 PubMed DOI PMC

Staudigl T, Vollmar C, Noachtar S, Hanslmayr S (2015) Temporal-pattern similarity analysis reveals the beneficial and detrimental effects of context reinstatement on human memory. J Neurosci 35:5373–5384. 10.1523/JNEUROSCI.4198-14.2015 PubMed DOI PMC

Tang C, Hamilton LS, Chang EF (2017) Intonational speech prosody encoding in the human auditory cortex. Science 357:797–801. 10.1126/science.aam8577 PubMed DOI PMC

Tourville JA, Guenther FH (2011) The DIVA model: a neural theory of speech acquisition and production. Lang Cogn Process 26:952–981. 10.1080/01690960903498424 PubMed DOI PMC

Waldhauser GT, Bäuml KH, Hanslmayr S (2015) Brain oscillations mediate successful suppression of unwanted memories. Cereb Cortex 25:4180–4190. 10.1093/cercor/bhu138 PubMed DOI

Wang XJ. (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195–1268. 10.1152/physrev.00035.2008 PubMed DOI PMC

Yaffe RB, Kerr MS, Damera S, Sarma SV, Inati SK, Zaghloul KA (2014) Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval. Proc Natl Acad Sci U S A 111:18727–18732. 10.1073/pnas.1417017112 PubMed DOI PMC