Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Intracerebral evidence of rhythm transform in the human auditory cortex

Abstract

Musical entrainment is shared by all human cultures and the perception of a periodic beat is a cornerstone of this entrainment behavior. Here, we investigated whether beat perception might have its roots in the earliest stages of auditory cortical processing. Local field potentials were recorded from 8 patients implanted with depth-electrodes in Heschl’s gyrus and the planum temporale (55 recording sites in total), usually considered as human primary and secondary auditory cortices. Using a frequency-tagging approach, we show that both low-frequency (<30 Hz) and high-frequency (>30 Hz) neural activities in these structures faithfully track auditory rhythms through frequency-locking to the rhythm envelope. A selective gain in amplitude of the response frequency-locked to the beat frequency was observed for the low-frequency activities but not for the high-frequency activities, and was sharper in the planum temporale, especially for the more challenging syncopated rhythm. Hence, this gain process is not systematic in all activities produced in these areas and depends on the complexity of the rhythmic input. Moreover, this gain was disrupted when the rhythm was presented at fast speed, revealing low-pass response properties which could account for the propensity to perceive a beat only within the musical tempo range. Together, these observations show that, even though part of these neural transforms of rhythms could already take place in subcortical auditory processes, the earliest auditory cortical processes shape the neural representation of rhythmic inputs in favor of the emergence of a periodic beat.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Bancaud J, Talairach J (1973) Methodology of stereo EEG exploration and surgical intervention in epilepsy. Rev Otoneuroophtalmol 45(4):315–328

  2. Brosch M, Budinger E, Scheich H (2002) Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol 87:2715–2725

  3. Brugge JF, Nourski KV, Oya H, Reale RA, Kawasaki H, Steinschneider M, Howard MA 3rd (2009) Coding of repetitive transients by auditory cortex on Heschl’s gyrus. J Neurophysiol 102(4):2358–2374

  4. Chemin B, Mouraux A, Nozaradan S (2014) Body movement selectively shapes the neural representation of musical rhythm. Psychol Sci 25(12):2147–2159

  5. Cirelli LK, Spinelli C, Nozaradan S, Trainor LJ (2016) Measuring neural entrainment to beat and meter in infants: effects of music background. Front Neurosci 10:229. doi:10.3389/fnins.2016.00229

  6. Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, Saenz M (2011) Human primary auditory cortex follows the shape of Heschl’s gyrus. J Neurosci 31(40):14067–14075

  7. Drake C, Botte MC (1993) Tempo sensitivity in auditory sequences: evidence for a multiple-look model. Percept Psychophys 54(3):277–286

  8. Drullman R, Festen JM, Plomp R (1994a) Effect of reducing slow temporal modulations on speech reception. J Acoust Soc Am 95:2670–2680

  9. Drullman R, Festen JM, Plomp R (1994b) Effect of temporal envelope smearing on speech reception. J Acoust Soc Am 95:1053–1064

  10. Edwards E, Chang EF (2013) Syllabic (~2–5 Hz) and fluctuation (~1–10 Hz) ranges in speech and auditory processing. Hear Res 305:113–134. doi:10.1016/j.heares.2013.08.017

  11. Eggermont JJ (2001) Between sound and perception: reviewing the search for a neural code. Hear Res 157(1–2):1–42

  12. Erulkar SD, Butler RA, Gerstein GL (1968) Excitation and inhibition in cochlear nucleus. II. Frequency modulated tones. J Neurophysiol 31:537–548

  13. Fernald RD, Gerstein GL (1972) Response of cat cochlear nucleus neurons to frequency and amplitude modulated tones. Brain Res 45:417–435

  14. Fraisse P (1967) Psychologie du temps. Presses universitaires de France, France

  15. Friedman-Hill S, Maldonado PE, Gray CM (2000) Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus dependence of gammaband neuronal oscillations. Cereb Cortex 10:1105–1116

  16. Frien A, Eckhorn R, Bauer R, Woelbern T, Gabriel A (2000) Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey. Eur J Neurosci 12:1453–1465

  17. Fujioka T, Trainor LJ, Large EW, Ross B (2012) Internalized timing of isochronous sounds is represented in neuromagnetic β oscillations. J Neurosci 32(5):1791–1802

  18. Gourévitch B, Le Bouquin Jeannès R, Faucon G, Liégeois-Chauvel C (2011) Temporal envelope processing in the human auditory cortex: response and interconnections of auditory cortical areas. Hear Res 237(1–2):1–18

  19. Grahn JA (2012) Neural mechanisms of rhythm perception: current findings and future perspectives. Top Cogn Sci 4(4):585–606

  20. Griffiths TD, Warren JD (2002) The planum temporale as a computational hub. Trends Neurosci 25(7):348–353

  21. Hove MJ, Risen JL (2009) It’s all in the timing: interpersonal synchrony increases affiliation. Soc Cogn 27:949–961

  22. Hove MJ, Marie C, Bruce IC, Trainor LJ (2014) Superior time perception for lower musical pitch explains why bass-ranged instruments lay down musical rhythms. Proc Natl Acad Sci USA 111(28):10383–10388

  23. Jonas J, Jacques C, Liu-Shuang J, Brissart H, Colnat-Coulbois S, Maillard L, Rossion B (2016) A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials. Proc Natl Acad Sci USA 113(28):E4088–E4097

  24. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84(2):541–577 (Review)

  25. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320(5872):110–113

  26. Large EW (2008) Resonating to musical rhythm: theory and experiment. In: Grondin Simon (ed) The psychology of time. Emerald, West Yorkshire

  27. Large EW (2010) Neurodynamics of music. In: Riess Jones M, Fay RR, Popper AN (eds) Springer handbook of auditory research, vol 36., Music perceptionSpringer, New York, pp 201–231

  28. Large EW, Herrera JA, Velasco MJ (2015) Neural networks for beat perception in musical rhythm. Front Syst Neurosci 25(9):159. doi:10.3389/fnsys.2015.00159

  29. Leonard MK, Bouchard KE, Tang C, Chang EF (2015) Dynamic encoding of speech sequence probability in human temporal cortex. J Neurosci 35(18):7203–7214

  30. Liégeois-Chauvel C, Lorenzi C, Trébuchon A, Régis J, Chauvel P (2004) Temporal envelope processing in the human left and right auditory cortices. Cereb Cortex 14(7):731–740

  31. London J (2004) Hearing in time: psychological aspects of musical meter. Oxford UP, London

  32. Malone BJ, Schreiner CE (2010) Time-varying sounds: amplitude envelope modulations. In: Rees A, Palmer AR (eds) The auditory brain. Oxford University Press, Oxford, New York, pp 125–148

  33. McAuley JD (2010) Tempo and rhythm. In Jones MR et al. (eds.) Music Perception, Springer Handbook of Auditory Research 36, USA

  34. Merchant H, Honing H (2014) Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Front Neurosci 7:274. doi:10.3389/fnins.2013.00274

  35. Miller KJ, Foster BL, Honey CJ (2012) Does rhythmic entrainment represent a generalized mechanism for organizing computation in the brain? Front Comput Neurosci 6:85

  36. Møller AR (1972) Coding of amplitude and frequency modulated sounds in the cochlear nucleus of the rat. Acta Physiol Scand 86:223–238

  37. Mouraux A, Iannetti GD, Colon E, Nozaradan S, Legrain V, Plaghki L (2011) Nociceptive steady-state evoked potentials elicited by rapid periodic thermal stimulation of cutaneous nociceptors. J Neurosci 31:6079–6087

  38. Norcia AM, Appelbaum LG, Ales JM, Cottereau BR, Rossion B (2015) The steady-state visual evoked potential in vision research: a review. J Vis 15(6):4

  39. 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(49):15564–15574

  40. Nourski KV, Steinschneider M, Rhone AE, Oya H, Kawasaki H, Howard MA 3rd, McMurray B (2015) Sound identification in human auditory cortex: differential contribution of local field potentials and high gamma power as revealed by direct intracranial recordings. Brain Lang 148:37–50

  41. Nozaradan S (2014) Exploring how musical rhythm entrains brain activity with electroencephalogram frequency-tagging. Philos Trans B 369(1658):20130393. doi:10.1098/rstb.2013.0393

  42. Nozaradan S, Peretz I, Missal M, Mouraux A (2011) Tagging the neuronal entrainment to beat and meter. J Neurosci 31:10234–10240

  43. Nozaradan S, Peretz I, Mouraux A (2012a) Steady-state evoked potentials as an index of multisensory temporal binding. Neuroimage 60(1):21–28

  44. Nozaradan S, Peretz I, Mouraux A (2012b) Selective neuronal entrainment to the beat and meter embedded in a musical rhythm. J Neurosci 32(49):17572–17581

  45. Nozaradan S, Zerouali Y, Peretz I, Mouraux A (2015) Capturing with EEG the neural entrainment and coupling underlying sensorimotor synchronization to the beat. Cereb Cortex 25(3):736–747

  46. Nozaradan S, Peretz I, Keller PE (2016a) Individual differences in rhythmic cortical entrainment correlate with predictive behavior in sensorimotor synchronization. Sci Rep 6:20612. doi:10.1038/srep20612

  47. Nozaradan S, Schönwiesner M, Caron-Desrochers L, Lehmann A (2016b) Enhanced brainstem and cortical encoding of sound during synchronized movement. Neuroimage 16:30322–30326

  48. Pantev C, Hoke M, Lehnertz K, Lütkenhöner B, Anogianakis G, Wittkowski W (1988) Tonotopic organization of the human auditory cortex revealed by transient auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 69(2):160–170

  49. 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

  50. Patel AD, Iversen JR (2014) The evolutionary neuroscience of musical beat perception: the Action Simulation for Auditory Prediction (ASAP) hypothesis. Front Psychol 8:57. doi:10.3389/fnsys.2014.00057

  51. Phillips-Silver J, Keller PE (2012) Searching for roots of entrainment and joint action in early musical interactions. Front Hum Neurosci 6:26

  52. Phillips-Silver J, Trainor LJ (2007) Hearing what the body feels: auditory encoding of rhythmic movement. Cognition 105(3):533–546

  53. Picton TW, Skinner CR, Champagne SC, Kellett AJ, Maiste AC (1987) Potentials evoked by the sinusoidal modulation of the amplitude or frequency of a tone. J Acoust Soc Am 82:165–178

  54. Povel DJ, Essens PJ (1985) Perception of temporal patterns. Music Percept 2:411–441

  55. Rajendran VG, Harper NS, Willmore BD, Schnupp JWH (2015) A biologically plausible model of beat detection in complex rhythmic sounds. In: Proceedings of the rhythm perception and production workshop, Amsterdam

  56. Regan DM (1989) Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine. Elsevier, New York

  57. Repp BH (2005) Sensorimotor synchronization: a review of the tapping literature. Psychon Bull Rev 12(6):969–992

  58. Repp BH, Su YH (2013) Sensorimotor synchronization: a review of recent research (2006–2012). Psychon Bull Rev 20(3):403–452. doi:10.3758/s13423-012-0371-2

  59. Rossion B (2014) Understanding individual face discrimination by means of fast periodic visual stimulation. Exp Brain Res 232(6):1599–1621

  60. Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32(1):9–18

  61. Shannon RV, Zeng F-G, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303–304

  62. Smith ZM, Delgutte B, Oxenham AJ (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876):87–90

  63. Steinschneider M, Fishman YI, Arezzo JC (2008) Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. Cereb Cortex 18(3):610–625

  64. Steinschneider M, Nourski KV, Kawasaki H, Oya H, Brugge JF, Howard MA 3rd (2011) Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21(10):2332–2347

  65. Steinschneider M, Nourski KV, Fishman YI (2013) Representation of speech in human auditory cortex: is it special? Hear Res 305:57–73

  66. Toiviainen P, Luck G, Thompson M (2010) Embodied meter: hierarchical eigenmodes in music-induced movement. Music Percept 28:59–70

  67. Tranchant P, Vuvan D (2015) Current conceptual challenges in the study of rhythm processing deficits. Front Neurosci 9:197. doi:10.3389/fnins.2015.00197

  68. van Noorden L, Moelants D (1999) Resonance in the perception of musical pulse. J New Music Res 28:43–66

  69. Velasco MJ, Large EW (2011) Pulse detection in syncopating rhythms using neural oscillators. In: Proceedings of the 12th annual conference of the international society for music information retrieval, pp 186–190

  70. Wang Y, Ding N, Ahmar N, Xiang J, Poeppel D, Simon JZ (2012) Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: MEG evidence. J Neurophysiol 107(8):2033–2041. doi:10.1152/jn.00310.2011

  71. Zatorre RJ, Chen JL, Penhune VB (2007) When the brain plays music: auditory-motor interactions in music perception and production. Nat Rev Neurosci 8(7):547–558

  72. Zion Golumbic EM, 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(5):980–991

Download references

Acknowledgements

S.N. is supported by an Australian Research Council (ARC) DECRA DE160101064 and by the Belgian National Fund for Scientific Research (F.R.S.-FNRS) FRSM 3.4558.12 Convention Grant (to Pr. A. Mouraux). J.J. and B.R. are supported by the Belgian National Fund for Scientific Research (F.R.S.-FNRS).

Author information

Correspondence to Sylvie Nozaradan.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nozaradan, S., Mouraux, A., Jonas, J. et al. Intracerebral evidence of rhythm transform in the human auditory cortex. Brain Struct Funct 222, 2389–2404 (2017). https://doi.org/10.1007/s00429-016-1348-0

Download citation

Keywords

  • Intracerebral EEG
  • Human auditory perception
  • Human depth-electrode recording
  • Music cognition
  • Frequency-tagging
  • Musical rhythm and beat processing