Experimental Brain Research

, Volume 135, Issue 2, pp 222–230 | Cite as

Conscious and preconscious adaptation to rhythmic auditory stimuli: a magnetoencephalographic study of human brain responses

  • F. Tecchio
  • C. Salustri
  • M. H. Thaut
  • P. Pasqualetti
  • P. M. Rossini
Research Article

Abstract

This study was triggered by the experimental evidence that subjects required to tap in synchrony with a heard rhythm spontaneously time their tapping to variations in rhythm frequency even when these variations are so small that they are not consciously detectable. We performed a series of magnetoencephalographic (MEG) measurements, aimed at investigating whether the response of the auditory cortex discriminates randomly administered series of brief tones differing from each other only by their interstimulus intervals (ISI). Moreover, by combining psychophysical measurements, conscious and preconscious adjustments of tapping to rhythm variations were compared with brain cortical responses. The ISIs were varied by 2% or 20% from a “central” value of 500 ms. Subjects always consciously detected the 20% ISI changes and easily adjusted their tapping accordingly, whereas they never consciously detected the 2% ISI changes, even though they always correctly adjusted their tapping to them. Analysis of the auditory evoked fields (AEFs) showed that the intensity of the M100 component decreased with decreasing ISI both for 20% and 2% variations in a statistically significant manner, despite the fact that the 2% variation was not consciously perceived. The M100 behavior indicated that connections between auditory and motor cortexes may exist that are able to use the information on rhythm variations in the stimuli even when these are not consciously identified by the subject. The ability of the auditory cortex to discriminate different time characteristics of the incoming rhythmic stimuli is discussed in this paper in relation to the theories regarding the physiology of time perception and discrimination.

Key words

Rhythm perception Auditory evoked fields Auditory-motor synchronization Human 

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References

  1. Berman IW (1981) Musical functioning, speech lateralization and the amusias. S Afr Med J 59:78–81PubMedGoogle Scholar
  2. Buonomano DV (2000) Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci 20:1129–1141PubMedGoogle Scholar
  3. Buonomano DV, Merzenich MM (1995) Temporal information transformed into a spatial code by a neural network with realistic properties. Science 267:1028–1030PubMedCrossRefGoogle Scholar
  4. Buonomano DV, Hickmott PW, Merzenich MM (1997) Context-sensitive synaptic plasticity and temporal-to-spatial transformations in hippocampal slices. Proc Natl Acad Sci USA 94:10403–10408PubMedCrossRefGoogle Scholar
  5. Collyer CE, Broadbent HA, Church RM (1992) Categorical time production: evidence for discrete timing in motor control. Percept Psychophys 51:134–144PubMedGoogle Scholar
  6. Cowan N (1984) On short and long auditory stores. Psychol Bull 96:341–370PubMedCrossRefGoogle Scholar
  7. Dawe LA, Piatt JR, Racine RJ (1995) Rhythm perception and differences in accent weights for musicians and non-musicians. Percept Psychophys 57:905–914PubMedGoogle Scholar
  8. Elberling C, Bak C, Kofoed B, Lebech J, Saermark K (1982) Auditory magnetic fields from the human cerebral cortex: location and strength of an equivalent current dipole. Acta Neurol Scand 65:553–569PubMedCrossRefGoogle Scholar
  9. Ernè SN, Narici L, Pizzella V, Romani GL (1987) The position problem in biomagnetic measurement: a solution for arrays of superconducting sensors IEEE Trans Magn 23:1319–1322CrossRefGoogle Scholar
  10. Fitzgibbons PJ, Pollatsek A, Thomas IB (1974) Detection of temporal gaps within and between perceptual tonal groups. Percept Psychophys 16:522–528Google Scholar
  11. Franek M, Mates J, Radii T, Beck K, Poppel E (1994) Sensorimotor synchronization: motor responses to pseudoregular auditory patterns. Percept Psychophys 55:204–217PubMedGoogle Scholar
  12. Fries W (1990) Disturbance of rhythm sense following right hemisphere damage. Neuropsychologia 28:1317–1323PubMedCrossRefGoogle Scholar
  13. Gallen C, Pantev C, Hampson S, Buchanan DS, Sobel D (1992) Reliability and validity of auditory neuromagnetic source localization using a large array biomagnetometer. In: Hoke M, Ernè SN, Okada YC, Romani GL (eds) Biomagnetism: clinical aspects. Excerpta Medica, Amsterdam, pp 171–175Google Scholar
  14. Hari R, Aittoniemi K, Jarvinen ML, Katila T, Varpula T (1980) Auditory evoked transient and sustained magnetic fields of the human brain: localization of neural generators. Exp Brain Res 40:237–240PubMedCrossRefGoogle Scholar
  15. Hari R, Kaila K, Kaila T, Tuomitso T, Varpula T (1982) Interstimulus dependence of the auditory vertex response and its magnetic counterpart: implications for their neural generation. Electroencephalogr Clin Neurophysiol 54:561–569PubMedCrossRefGoogle Scholar
  16. Hari R, Pelizzone M, Makela PJ, Hallstrom J, Leinonen L, Lounasmaa OV (1987) Neuromagnetic responses of the human auditory cortex to on- and offsets to noise bursts Audiology 26:31–43PubMedCrossRefGoogle Scholar
  17. Hari R, Joutsiniemi SL, Hamalainen M, Vilkman V (1989) Neuromagnetic responses of human auditory cortex to interruptions in a steady rhythm. Neurosci Lett 99:164–168PubMedCrossRefGoogle Scholar
  18. Imada T, Watanabe M, Mashiko T, Kawakatsu M, Kotani M (1997) The silent period between sounds has a stronger effect than the interstimulus interval on auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 102:37–45PubMedCrossRefGoogle Scholar
  19. Ivry RB, Keele SW (1989) Timing functions of the cerebellum. J Cogn Neurosci 1:134–150CrossRefGoogle Scholar
  20. Joutsiniemi SL, Hari R (1989) Omissions of auditory stimuli may activate frontal cortex. Eur J Neurosci 1:524–528PubMedCrossRefGoogle Scholar
  21. Kagerer F, Ilmberger J, Poppel E, Mates J, Radii T (1990) Auditory motor synchronization: timing in incremental and decremental rhythmic tapping. Act Nerv Super 32:145–146Google Scholar
  22. Kraus N, Smith DI, McGee T (1988) Midline and temporal lobe MLRs in the guinea pig originate from different generator systems: a conceptual framework for new and existing data. Electroencephalogr Clin Neurophysiol 70:541–558PubMedCrossRefGoogle Scholar
  23. Lang W, Obrig H, Lindinger G, Cheyne D, Deeke L (1990) Supplementary motor area activation while tapping bimanually different rhythms in musicians. Exp Brain Res 79:504–514PubMedCrossRefGoogle Scholar
  24. Levanen S, Ahonen A, Hari R, McEvoy L, Sams M (1996) Deviant auditory stimuli activate human left and right auditory cortex differently. Cereb Cortex 6:288–96PubMedCrossRefGoogle Scholar
  25. Lu ZL, Williamson SJ, Kaufman L (1992a) Human auditory primary and association cortex have different lifetimes for activation traces. Brain Res 572:236–241PubMedCrossRefGoogle Scholar
  26. Lu ZL, Williamson SJ, Kaufman L (1992b) Behavioral lifetime of human auditory sensory memory predicted by physiological measures. Science 258:1668–1670PubMedCrossRefGoogle Scholar
  27. Makela JP, Hari R, Linnankivi A (1987) Different analysis of frequency and amplitude modulations of a continuous tone in the human auditory cortex: a neuromagnetic study. Hearing Res 27:257–264CrossRefGoogle Scholar
  28. Mayville JM, Bressler SL, Fuchs A, Kelso JA (1999) Spatiotemporal reorganization of electrical activity in the human brain associated with a timing transition in rhythmic auditory-motor coordination. Exp Brain Res 127:371–81PubMedCrossRefGoogle Scholar
  29. Meek WH, Church RM (1987) Nutrients modify the speed of internal clock and memory stages processes. Behav Neurosci 101:465–475CrossRefGoogle Scholar
  30. Melvill Jones G, Watt DGD (1971) Observations on the control of stepping and hopping movements in man. J Physiol (Lond) 219:709–727Google Scholar
  31. Miller RA, Thaut MH, Aunon JI (1994) Event related brain wave potentials in an auditory-motor synchronization task. In: Pratt RR, Spintge R (eds) Music medicine. MMB Music, St Louis, pp 76–84Google Scholar
  32. Monahan CB, Hirsh IJ (1990) Studies in auditory timing. 2. Rhythm patterns. Percept Psychophys 47:227–242PubMedGoogle Scholar
  33. Pantev C, Hoke M, Luntkenhoner B, Fahrendorf G, Stober U (1990) Identification of sources of brain neuronal activity with high spatiotemporal resolution through combination of neuromagnetic source localization (NMSL) and magnetic resonance imaging (MRI). Electroencephalogr Clin Neurophysiol 75:173–184PubMedCrossRefGoogle Scholar
  34. Pantev C, Elbert T, Makeig S, Hampson S, Eulitz C, Hoke M (1993) Relationship of transient and steady-state auditory evoked fields. Electroencephalogr Clin Neurophysiol 88:389–396PubMedCrossRefGoogle Scholar
  35. Papanicolau AC, Banmann S (1990) Localization of auditory responses sources using MEG and MRI. Arch Neurol 47:33Google Scholar
  36. Pellizzone M, Hari R, Makela JP, Huttunen J, Ahlfors S, Hamalainen M (1987) Cortical origin of the middle latency auditory evoked responses in man. Neurosci Lett 82:303–307CrossRefGoogle Scholar
  37. Povel DJ, Essen P (1985) Perception of temporal patterns. Music Percept 2:411–440Google Scholar
  38. Rao SM, Harrington DL, Haaland KY, Bobholz JA, Cox RW, Binder JR (1997) Distributed neural systems underlying the timing of movements. J Neurosci 17:5528–5535PubMedGoogle Scholar
  39. Reite M, Edrich J, Zimmerman JT, Zimmerman JE (1978) Human magnetic auditory evoked fields. Electroencephalogr Clin Neurophysiol 45:114–117PubMedCrossRefGoogle Scholar
  40. Romani GL, Williamson SJ, Kaufmann L (1982) Tonotopic organization of the human auditory cortex. Science 216:1339–1340PubMedCrossRefGoogle Scholar
  41. Ross J, Houtsma AJM (1994) Discrimination of auditory temporal patterns. Percept Psychophys 56:19–26PubMedGoogle Scholar
  42. Rossignol S, Melvill Jones G (1976) Audio-spinal influence in man studied by the H-reflex and its possible role on rhythmic movements synchronized to sound. Electroencephalogr Clin Neurophysiol 41:83–92PubMedCrossRefGoogle Scholar
  43. Sams M, Kaukoranta E, Hamalainen M, Naatanen R (1991) Cortical activity elicited by changes in auditory stimuli. Psychophysiology 28:21–28PubMedCrossRefGoogle Scholar
  44. Sams M, Hari R, Rif J, Knutila J (1993) The human auditory sensory memory trace persists about 10 s: neuromagnetic evidence. J Cogn Neurosci 5:363–370CrossRefGoogle Scholar
  45. Tecchio F, Rossini PM, Pizzella V, Cassetta E, Romani G-L (1997) Spatial properties and interhemispheric differences of the sensory hand cortical representation: a neuromagnetic study. Brain Res 767:100–108PubMedCrossRefGoogle Scholar
  46. Thaut MH, Miller RA, Schauer ML (1998) Multiple synchronization strategies in rhythmic sensorimotor tasks: phase vs period corrections. Biol Cybern 79:241–250PubMedCrossRefGoogle Scholar
  47. Treisman M, Cook N, Naish PLN, MacCrone JK (1994) The internal clock: electroencephalographic evidence for oscillatory time perception. Q J Exp Psychol A 47:241–289PubMedGoogle Scholar
  48. Vos PG, Mates J, Kruysbergen NW (1995) The perceptual centre of a stimulus as the cue for synchronization to a metronome: evidence from asynchronies. Q J Exp Psychol A 48:1024–1040PubMedGoogle Scholar
  49. Wearden JH, Penton-Voak IS (1995) Feeling the heat: body temperature and the rate of subjective time, revisited. Q J Exp Psychol 48:129–141Google Scholar
  50. West MO, Peoples LL, Michael AJ, Chapin JK, Woodward DJ (1997) Low-dose amphetamine elevates movement-related firing of rat striatal neurons. Brain Res 745:331–335PubMedCrossRefGoogle Scholar
  51. Woods DL, Clayworth CC, Knight RT, Simpson GV, Naeser MA (1987) Generators of middle- and long-latency auditory evoked potentials: implications from studies of patients with bitemporal lesions. Electroencephalogr Clin Neurophysiol 68:132–148PubMedCrossRefGoogle Scholar
  52. Woodward DJ, Janak PH, Chang JY (1998) Ethanol action on neural networks studied with multineuron recording in freely moving animals. Alcohol Clin Exp Res 22:10–22PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2000

Authors and Affiliations

  • F. Tecchio
    • 1
    • 4
  • C. Salustri
    • 1
    • 4
  • M. H. Thaut
    • 2
    • 3
    • 5
  • P. Pasqualetti
    • 4
    • 6
  • P. M. Rossini
    • 4
    • 5
    • 6
  1. 1.IESS-CNRUnita MEG-Ospedale FatebenefratelliRomeItaly
  2. 2.Department of MusicColorado State UniversityUSA
  3. 3.Department Electrical EngineeringColorado State UniversityUSA
  4. 4.FaR-Div. NeuroscienzeOspedale FatebenefratelliRomeItaly
  5. 5.IRCCS “S. Lucia”RomeItaly
  6. 6.IRCCS “S. Giovanni di Dio-F.B.F”BresciaItaly

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