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Laminar specificity of oscillatory coherence in the auditory cortex

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Abstract

Empirical evidence suggests that, in the auditory cortex (AC), the phase relationship between spikes and local-field potentials (LFPs) plays an important role in the processing of auditory stimuli. Nevertheless, unlike the case of other sensory systems, it remains largely unexplored in the auditory modality whether the properties of the cortical columnar microcircuit shape the dynamics of spike–LFP coherence in a layer-specific manner. In this study, we directly tackle this issue by addressing whether spike–LFP and LFP–stimulus phase synchronization are spatially distributed in the AC during sensory processing, by performing laminar recordings in the cortex of awake short-tailed bats (Carollia perspicillata) while animals listened to conspecific distress vocalizations. We show that, in the AC, spike–LFP and LFP–stimulus synchrony depend significantly on cortical depth, and that sensory stimulation alters the spatial and spectral patterns of spike–LFP phase-locking. We argue that such laminar distribution of coherence could have functional implications for the representation of naturalistic auditory stimuli at a cortical level.

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References

  • Arnal LH, Giraud AL (2012) Cortical oscillations and sensory predictions. Trends Cogn Sci 16:390–398

    Article  PubMed  Google Scholar 

  • Atilgan H, Town SM, Wood KC, Jones GP, Maddox RK, Lee AKC, Bizley JK (2018) Integration of visual information in auditory cortex promotes auditory scene analysis through multisensory binding. Neuron 97(640–655):e644

    Google Scholar 

  • Barczak A, O’Connell MN, McGinnis T, Ross D, Mowery T, Falchier A, Lakatos P (2018) Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit. Proc Natl Acad Sci USA 115:E7605–E7614

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76:695–711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beltramo R, D’Urso G, Dal Maschio M, Farisello P, Bovetti S, Clovis Y, Lassi G, Tucci V, De Pietri Tonelli D, Fellin T (2013) Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat Neurosci 16:227–234

    Article  PubMed  CAS  Google Scholar 

  • Berens P (2009) CircStat: a MATLAB toolbox for circular statistics. J Stat Softw 31:1–21

    Article  Google Scholar 

  • Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: a platform for analyzing neural signals. J Neurosci Methods 192:146–151

    Article  PubMed  PubMed Central  Google Scholar 

  • Buffalo EA, Fries P, Landman R, Buschman TJ, Desimone R (2011) Laminar differences in gamma and alpha coherence in the ventral stream. Proc Natl Acad Sci USA 108:11262–11267

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Buzsaki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Buzsaki G, Anastassiou CA, Koch C (2012) The origin of extracellular fields and currents—EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13:407–420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Creutzfeldt O, Hellweg FC, Schreiner C (1980) Thalamocortical transformation of responses to complex auditory stimuli. Exp Brain Res 39:87–104

    Article  PubMed  CAS  Google Scholar 

  • De Martino F, Moerel M, Ugurbil K, Goebel R, Yacoub E, Formisano E (2015) Frequency preference and attention effects across cortical depths in the human primary auditory cortex. Proc Natl Acad Sci USA 112:16036–16041

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Doelling KB, Assaneo MF, Bevilacqua D, Pesaran B, Poeppel D (2019) An oscillator model better predicts cortical entrainment to music. Proc Natl Acad Sci USA 116:10113–10121

    PubMed  CAS  PubMed Central  Google Scholar 

  • Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419–451

    Article  PubMed  CAS  Google Scholar 

  • Einevoll GT, Kayser C, Logothetis NK, Panzeri S (2013) Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat Rev Neurosci 14:770–785

    Article  PubMed  CAS  Google Scholar 

  • Esser KH, Eiermann A (1999) Tonotopic organization and parcellation of auditory cortex in the FM-bat Carollia perspicillata. Eur J Neurosci 11:3669–3682

    Article  PubMed  CAS  Google Scholar 

  • Farahani ED, Goossens T, Wouters J, van Wieringen A (2017) Spatiotemporal reconstruction of auditory steady-state responses to acoustic amplitude modulations: potential sources beyond the auditory pathway. Neuroimage 148:240–253

    Article  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

    Article  PubMed  CAS  Google Scholar 

  • Francis NA, Elgueda D, Englitz B, Fritz JB, Shamma SA (2018) Laminar profile of task-related plasticity in ferret primary auditory cortex. Sci Rep 8:16375

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224

    Article  PubMed  CAS  Google Scholar 

  • Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88:220–235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Wehr M (2015) A coding transformation for temporally structured sounds within auditory cortical neurons. Neuron 86:292–303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao L, Kostlan K, Wang Y, Wang X (2016) Distinct subthreshold mechanisms underlying rate-coding principles in primate auditory cortex. Neuron 91:905–919

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Rosales F, Beetz MJ, Cabral-Calderin Y, Kössl M, Hechavarria JC (2018a) Neuronal coding of multiscale temporal features in communication sequences within the bat auditory cortex. Commun Biol 1:200

    Article  PubMed  PubMed Central  Google Scholar 

  • García-Rosales F, Martin LM, Beetz MJ, Cabral-Calderin Y, Kossl M, Hechavarria JC (2018b) Low-frequency spike-field coherence is a fingerprint of periodicity coding in the auditory cortex. iScience 9:47–62

    Article  PubMed  PubMed Central  Google Scholar 

  • Giraud AL, Poeppel D (2012) Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15:511–517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Haegens S, Handel BF, Jensen O (2011) Top-down controlled alpha band activity in somatosensory areas determines behavioral performance in a discrimination task. J Neurosci 31:5197–5204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haider B, Schulz DP, Hausser M, Carandini M (2016) Millisecond coupling of local field potentials to synaptic currents in the awake visual cortex. Neuron 90:35–42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hansen BJ, Dragoi V (2011) Adaptation-induced synchronization in laminar cortical circuits. Proc Natl Acad Sci USA 108:10720–10725

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Harris KD, Mrsic-Flogel TD (2013) Cortical connectivity and sensory coding. Nature 503:51–58

    Article  PubMed  CAS  Google Scholar 

  • Hechavarria JC, Beetz MJ, Macias S, Kossl M (2016a) Distress vocalization sequences broadcasted by bats carry redundant information. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 202:503–515

    Article  PubMed  Google Scholar 

  • Hechavarria JC, Beetz MJ, Macias S, Kossl M (2016b) Vocal sequences suppress spiking in the bat auditory cortex while evoking concomitant steady-state local field potentials. Sci Rep 6:39226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Henry MJ, Obleser J (2012) Frequency modulation entrains slow neural oscillations and optimizes human listening behavior. Proc Natl Acad Sci USA 109:20095–20100

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Herdman AT, Lins O, Van Roon P, Stapells DR, Scherg M, Picton TW (2002) Intracerebral sources of human auditory steady-state responses. Brain Topogr 15:69–86

    Article  PubMed  Google Scholar 

  • Hyafil A, Fontolan L, Kabdebon C, Gutkin B, Giraud AL (2015) Speech encoding by coupled cortical theta and gamma oscillations. Elife 4:e06213

    Article  PubMed  PubMed Central  Google Scholar 

  • Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577

    Article  PubMed  CAS  Google Scholar 

  • Kayser C, Petkov CI, Logothetis NK (2008) Visual modulation of neurons in auditory cortex. Cereb Cortex 18:1560–1574

    Article  PubMed  Google Scholar 

  • Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597–608

    Article  PubMed  CAS  Google Scholar 

  • Kayser C, Ince RA, Panzeri S (2012) Analysis of slow (theta) oscillations as a potential temporal reference frame for information coding in sensory cortices. PLoS Comput Biol 8:e1002717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Konig P, Engel AK, Singer W (1995) Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc Natl Acad Sci USA 92:290–294

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94:1904–1911

    Article  PubMed  Google Scholar 

  • Lakatos P, Chen CM, O’Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lakatos P, Musacchia G, O’Connel MN, Falchier AY, Javitt DC, Schroeder CE (2013) The spectrotemporal filter mechanism of auditory selective attention. Neuron 77:750–761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Levy JM, Zold CL, Namboodiri VMK, Hussain Shuler MG (2017) The timing of reward-seeking action tracks visually cued theta oscillations in primary visual cortex. J Neurosci 37:10408–10420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Linden JF, Schreiner CE (2003) Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb Cortex 13:83–89

    Article  PubMed  Google Scholar 

  • Luo H, Poeppel D (2007) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54:1001–1010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo H, Liu Z, Poeppel D (2010) Auditory cortex tracks both auditory and visual stimulus dynamics using low-frequency neuronal phase modulation. PLoS Biol 8:e1000445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manita S, Suzuki T, Homma C, Matsumoto T, Odagawa M, Yamada K, Ota K, Matsubara C, Inutsuka A, Sato M et al (2015) A top-down cortical circuit for accurate sensory perception. Neuron 86:1304–1316

    Article  PubMed  CAS  Google Scholar 

  • Molinaro N, Lizarazu M (2018) Delta(but not theta)-band cortical entrainment involves speech-specific processing. Eur J Neurosci 48:2642–2650

    Article  PubMed  Google Scholar 

  • Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120(Pt 4):701–722

    Article  PubMed  Google Scholar 

  • Ng BSW, Schroeder T, Kayser C (2012) A precluding but not ensuring role of entrained low-frequency oscillations for auditory perception. J Neurosci 32:12268–12276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nourski KV, Brugge JF (2011) Representation of temporal sound features in the human auditory cortex. Rev Neurosci 22:187–203

    Article  PubMed  Google Scholar 

  • O’Connell MN, Barczak A, Schroeder CE, Lakatos P (2014) Layer specific sharpening of frequency tuning by selective attention in primary auditory cortex. J Neurosci 34:16496–16508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Connell MN, Barczak A, Ross D, McGinnis T, Schroeder CE, Lakatos P (2015) Multi-scale entrainment of coupled neuronal oscillations in primary auditory cortex. Front Hum Neurosci 9:655

    Article  PubMed  PubMed Central  Google Scholar 

  • Panzeri S, Brunel N, Logothetis NK, Kayser C (2010) Sensory neural codes using multiplexed temporal scales. Trends Neurosci 33:111–120

    Article  PubMed  CAS  Google Scholar 

  • Park H, Ince RA, Schyns PG, Thut G, Gross J (2015) Frontal top-down signals increase coupling of auditory low-frequency oscillations to continuous speech in human listeners. Curr Biol 25:1649–1653

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Percival DB, Walden AT (1993) Spectral analysis for physical applications. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reimann MW, Anastassiou CA, Perin R, Hill SL, Markram H, Koch C (2013) A biophysically detailed model of neocortical local field potentials predicts the critical role of active membrane currents. Neuron 79:375–390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romano J, Kromrey JD, Coraggio J, Skowronek J (2006) Appropriate statistics for ordinal level data: Should we really be using t-test and Cohen’s d for evaluating group differences on the NSSE and other surveys. Paper presented at: annual meeting of the Florida Association of Institutional Research

  • Romanski LM, LeDoux JE (1993) Organization of rodent auditory cortex: anterograde transport of PHA-L from MGv to temporal neocortex. Cereb Cortex 3:499–514

    Article  PubMed  CAS  Google Scholar 

  • Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903–907

    Article  PubMed  CAS  Google Scholar 

  • Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64:404–418

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027–1034

    Article  PubMed  CAS  Google Scholar 

  • Schaefer MK, Hechavarria JC, Kossl M (2015) Quantification of mid and late evoked sinks in laminar current source density profiles of columns in the primary auditory cortex. Front Neural Circuits 9:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaefer MK, Kossl M, Hechavarria JC (2017) Laminar differences in response to simple and spectro-temporally complex sounds in the primary auditory cortex of ketamine-anesthetized gerbils. PLoS One 12:e0182514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9–18

    Article  PubMed  CAS  Google Scholar 

  • Schroeder CE, Lakatos P, Kajikawa Y, Partan S, Puce A (2008) Neuronal oscillations and visual amplification of speech. Trends Cogn Sci 12:106–113

    Article  PubMed  PubMed Central  Google Scholar 

  • Spyropoulos G, Bosman CA, Fries P (2018) A theta rhythm in macaque visual cortex and its attentional modulation. Proc Natl Acad Sci USA 115:E5614–E5623

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stefanics G, Hangya B, Hernadi I, Winkler I, Lakatos P, Ulbert I (2010) Phase entrainment of human delta oscillations can mediate the effects of expectation on reaction speed. J Neurosci 30:13578–13585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Szymanski FD, Rabinowitz NC, Magri C, Panzeri S, Schnupp JW (2011) The laminar and temporal structure of stimulus information in the phase of field potentials of auditory cortex. J Neurosci 31:15787–15801

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang J, Suga N (2008) Modulation of auditory processing by cortico-cortical feed-forward and feedback projections. Proc Natl Acad Sci USA 105:7600–7605

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Teng X, Tian X, Rowland J, Poeppel D (2017) Concurrent temporal channels for auditory processing: oscillatory neural entrainment reveals segregation of function at different scales. PLoS Biol 15:e2000812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tiesinga P, Sejnowski TJ (2009) Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron 63:727–732

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Atteveldt N, Murray MM, Thut G, Schroeder CE (2014) Multisensory integration: flexible use of general operations. Neuron 81:1240–1253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Kerkoerle T, Self MW, Dagnino B, Gariel-Mathis MA, Poort J, van der Togt C, Roelfsema PR (2014) Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc Natl Acad Sci USA 111:14332–14341

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • van Wassenhove V, Grant KW, Poeppel D (2005) Visual speech speeds up the neural processing of auditory speech. Proc Natl Acad Sci USA 102:1181–1186

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • von Stein A, Chiang C, Konig P (2000) Top-down processing mediated by interareal synchronization. Proc Natl Acad Sci USA 97:14748–14753

    Article  Google Scholar 

  • Winer JA, Lee CC (2007) The distributed auditory cortex. Hear Res 229:3–13

    Article  PubMed  PubMed Central  Google Scholar 

  • Womelsdorf T, Fries P (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17:154–160

    Article  PubMed  CAS  Google Scholar 

  • Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609–1612

    Article  PubMed  CAS  Google Scholar 

  • Zion Golumbic EM, Poeppel D, Schroeder CE (2012) Temporal context in speech processing and attentional stream selection: a behavioral and neural perspective. Brain Lang 122:151–161

    Article  PubMed  PubMed Central  Google Scholar 

  • Zion Golumbic E, Cogan GB, Schroeder CE, Poeppel D (2013) Visual input enhances selective speech envelope tracking in auditory cortex at a “cocktail party”. J Neurosci 33:1417–1426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zoefel B, Heil P (2013) Detection of near-threshold sounds is independent of eeg phase in common frequency bands. Front Psychol 4:262

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by the German Research Council (DFG) (Grant no. HE 7478/1-1, to JCH). The authors would like to thank Gisa Prange for providing support with the histological approaches.

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Authors and Affiliations

  1. Institut für Zellbiologie und Neurowissenschaft, Goethe-Universität, Max-von-Laue-Str. 13, 60438, Frankfurt/Main, Germany

    Francisco García-Rosales, Dennis Röhrig, Kristin Weineck, Mira Röhm, Yi-Hsuan Lin, Manfred Kössl & Julio C. Hechavarria

  2. Research Group Neural and Environmental Rhythms, Max Planck Institute for Empirical Aesthetics, 60322, Frankfurt/Main, Germany

    Yuranny Cabral-Calderin

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  1. Francisco García-Rosales
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  2. Dennis Röhrig
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  5. Yi-Hsuan Lin
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  6. Yuranny Cabral-Calderin
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  7. Manfred Kössl
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  8. Julio C. Hechavarria
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Contributions

FGR and JCH designed the study. FGR, KW, MR and YHL collected the data. FGR analyzed the data and wrote the manuscript. FGR, DR, KW, MR, YHL, YCC, MK, and JCH discussed, interpreted the results, and reviewed the manuscript.

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Correspondence to Francisco García-Rosales or Julio C. Hechavarria.

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The authors declare no competing financial or non-financial interests.

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The data that support the findings of this study are available from the corresponding authors upon reasonable request.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All experimental procedures were in compliance with current European regulations on animal experimentation, and were approved by the Regierungspräsidium Darmstadt (experimental permit #FU-1126).

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García-Rosales, F., Röhrig, D., Weineck, K. et al. Laminar specificity of oscillatory coherence in the auditory cortex. Brain Struct Funct 224, 2907–2924 (2019). https://doi.org/10.1007/s00429-019-01944-3

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