Abstract
The objective of this study was to localize the intracerebral generators for auditory steady-state responses. The stimulus was a continuous 1000-Hz tone presented to the right or left ear at 70 dB SPL. The tone was sinusoidally amplitude-modulated to a depth of 100% at 12, 39, or 88 Hz. Responses recorded from 47 electrodes on the head were transformed into the frequency domain. Brain electrical source analysis treated the real and imaginary components of the response in the frequency domain as independent samples. The latency of the source activity was estimated from the phase of the source waveform. The main source model contained a midline brainstem generator with two components (one vertical and lateral) and cortical sources in the left and right supratemporal plane, each containing tangential and radial components. At 88 Hz, the largest activity occurred in the brainstem and subsequent cortical activity was minor. At 39 Hz, the initial brainstem component remained and significant activity also occurred in the cortical sources, with the tangential activity being larger than the radial. The 12-Hz responses were small, but suggested combined activation of both brainstem and cortical sources. Estimated latencies decreased for all source waveforms as modulation frequency increased and were shorter for the brainstem compared to cortical sources. These results suggest that the whole auditory nervous system is activated by modulated tones, with the cortex being more sensitive to slower modulation frequencies.
Similar content being viewed by others
References
Alain, C., Woods, D.L. and Ogawa, K.H. Brain indices of automatic pattern processing. NeuroReport, 1994, 6: 140–144.
Aoyagi, M., Kiren, T., Kim, Y., Suzuki, Y., Fuse, T. and Koike, Y. Optimalmodulation frequency for amplitude-modulation following response in young children during sleep. Hear. Res., 1993, 65: 253–261.
Arezzo, J., Pickoff, A. and Vaughan, H.G. The sources and intracerebral distribution of auditory evoked potentials in the alert rhesus monkey. Brain Res., 1975, 90: 57–73.
Azzena, G.B., Conti, G., Santarelli, R., Ottaviani, F., Paludetti, G. and Maurizi, M. Generation of human auditory steady-state responses (SSRs). I. Stimulus rate effects. Hear. Res., 1995, 83: 1–8.
Basar, E., Rosen, B., Basar-Eroglu, C. and Greitschus, F. The associations between 40-Hz and the middle latency response of the auditory evoked potential. J. Neurosci., 1987, 33: 103–117.
Batra, R., Kuwada, S. and Stanford, T.R. Temporal coding of envelopes and their interaural delays in the inferior colliculus of unanesthesized rabbit. J. Acoust. Soc. Am., 1989, 74: 257–268.
Berg, P. and Scherg, M. A fast method for forward computation of multiple-shell spherical head models. Electroencephalogr. Clin. Neurophysiol., 1994, 90: 58–64.
Brinkmann, R.D. and Scherg, M. Human auditory on-and offpotentials of the brainstem: influence of stimulus envelope charateristics. Scand. Audiol., 1979, 8: 27–32.
Cohen, L.T., Rickards, F.W. and Clark, G.M. A comparison of steady-state evoked potentials to modulated tones in awake and sleeping humans. J. Acoust. Soc. Am., 1991, 90: 2467–2479.
Creutzfeldt, O., Hellweg, F.C. and Schreiner, C. Thalamocortical transformation of responses to complex auditory stimuli. Exp. Brain Res., 1980, 39: 87–104.
Dobie, R.A. and Wilson, M.J. Low-level steady-state auditory evoked potentials: effects of rate and sedation on detectability. J. Acoust. Soc. Am., 1998, 104: 3482–3488.
Fastl, H., Hesse, A., Schorer, E., Urbas, J. and Muller-Preuss, P. Searching for neural correlates of the hearing sensation fluctuation strength in the auditory cortex of squirrelmonkeys. Hear. Res., 1986, 23: 199–203.
Firsching, R., Luther, J., Eidelberg, E., Brown, W.E., Jr., Story, J.L. and Boop, F.A. 40 Hz-middle latency auditory evoked response in comatose patients. Electroencephalogr. Clin. Neurophysiol., 1987, 67: 213–216.
Fischer, C., Bognar, L., Turjman, F. and Lapras, C. Auditory evoked potentials in a patient with a unilateral lesion of the inferior colliculus and medial geniculate body. Electroencephalogr. Clin. Neurophysiol., 1995, 96: 261–267.
Frisina, R.D., Smith, R.L. and Chamberlin, S.C. Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement. Hear. Res., 1990, 44: 99–122.
Galambos, R., Makeig, S. and Talmachoff, P.J. A40-Hz auditory potential recorded from the human scalp. Proc. Natl. Acad. Sci. U.S.A., 1981, 78: 2643–2647.
Gibson, W.P.R. Acoustically mediated brainstem reflexes. In: H.A. Beagley (Ed.), Auditory investigation: the scientific and technological basis. Oxford University Press, Oxford, 1979:302–323.
Gutschalk, A., Mase, R., Roth, R., Ille, N., Rupp, A., Hahnel, S., Picton, T.W. and Scherg, M. Deconvolution of 40 Hz steady-state fields reveals two overlapping source activities of the human auditory cortex. Clin. Neurophysiol., 1999, 110: 856–868.
Hari, R., Hämäläinen, M. and Joutsiniemi, S.L. Neuromagnetic steady-state responses to auditory stimuli. J. Acoust. Soc. Am., 1989, 86: 1033–1039.
Hashimoto, I., Mashiko, T., Yoshikawa, K., Mitzuta, T., Imada, T. and Hayashi, M. Neuromagnetic measurements of the human primary auditory response. Electroencephalogr. Clin. Neurophysiol., 1995, 96: 348–356
Herdman, A.T. and Stapells, D.R. Thresholds determined using the monotic and dichotic multiple auditory steady-state response technique in normal-hearing subjects. Scand. Audiol., 2001, 30: 41–49.
Jacobson, G. P., Privitera, M., Neils, J.R., Grayson, A. S. and Yeh, H. The effects of anterior temporal lobectomy (ATL) on the middle-latency auditory evoked potential (MLAEP). Electroencephalogr. Clin. Neurophysiol., 1990, 75: 230–241.
John, M.S. and Picton, T.W. Human auditory steady-state responses to amplitude-modulated tones: Phase and latency measurements. Hear. Res., 2000, 141: 57–79.
Johnson, B.W., Weinberg, H., Ribary, U., Cheyne, D.O. and Ancill, R. Topographic distribution of the 40 Hz auditory evoked-related potential in normal and aged subjects. Brain Topogr., 1988, 1: 117–121.
Kiren, T., Aoyagi, M., Furuse, H. and Koike, Y. An experimental study on the generator of amplitude-modulation following response]. Acta Otolaryng. Suppl. (Stockh.), 1994, 511: 28–33.
Knight, R.T. and Brailowsky, S. Auditory evoked potentials from the primary auditory cortex of the cat: topographic and pharmacological studies. Electroencephalogr. Clin. Neurophysiol., 1990, 77: 225–232.
Kraus, N., Ozdamar, O., Hier, D. and Stein, L. Auditory middle latency responses (MLRs) in patients with cortical lesions. Electroencephalogr. Clin. Neurophysiol., 1982, 54: 275–287.
Kraus, N., Smith, D.I. and McGee, T. 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., 1988, 70: 541–558.
Kuriki, S., Nogai, T. and Hirata, Y. Cortical sources of middle latency responses of auditory evoked magnetic field. Hear. Res., 1995, 92: 47–51.
Kuwada, S., Batra, R. and Maher, V.L. Scalp potentials of normal and hearing-impaired subjects in response to sinusoidally amplitude-modulated tones. Hear. Res., 1986, 21: 179–192.
Kuwada, S., Anderson, J.S., Batra, R., Fitzpatrick, D.C., Teissier, N. and D'Angelo, W.R. Sources of the scalp-recorded amplitude-modulation folling response. J. Amer. Acad. Audiol., 2002, 13: 188–204.
Lehmann, D. and Michel, C.M. Intracerebral dipole sources of EEG FFT power maps. Brain Topogr., 1989, 2: 155–164.
Lehmann, D. and Michel, C.M. Intracerebral dipole source localization for FFT power maps. Electroencephalogr. Clin. Neurophysiol., 1990, 76: 271–276.
Liégeois-Chauvel, C., Musolino, A., Badier, J.M., Marquis, P. and Chauvel, P. Evoked potentials recorded form the auditory cortex in man: evaluation and topography of the middle latency components. Electroencephalogr. Clin. Neurophysiol., 1994, 92: 204–214.
Linden, R.D., Campbell, K.B., Hamel, G. and Picton, T.W. Human auditory steady-state evoked potentials during sleep. Ear Hear., 1985, 6: 167–174.
Littman, T., Kraus, N., McGee, T. and Nicol, T. Binaural stimulation reveals functional differences between midline and temporal components of the middle latency response in guinea pigs. Electroencephalogr. Clin. Neurophysiol., 1992, 84: 362–372.
Mäkelä, J.P. and Hari, R. Evidence for cortical origin of the 40 Hz auditory evoked response in man. Electroencephalogr. Clin. Neurophysiol., 1987, 66: 539–546.
Mauer, G. and Döring, W.H. Generators of amplitude modulation following response (AMFR). Paper presented at 16th meeting of the Evoked Response Audiometry Study Group, Tromsø , Norway, June, 1999.
Maurizi, M., Almadori, G., Paludetti, G., Ottaviani, F., Rosignoli, M. and Luciano, R. 40-Hz steady-state response in newborns and in children. Audiology, 1990, 29: 322–328.
Mø ller, A.R. Dynamic properties of primary auditory nerve fibers compared with cells in the cochlear nucleus. Acta Physiol. Scand., 1976, 86: 223–228.
Pantev, C., Elbert, T., Makeig, S., Hampson, S., Eulitz, C. and Hoke, M. Relationship of transient and steady-state auditory evoked fields. Electroencephalogr. Clin. Neurophysiol., 1993, 88: 389–396.
Pantev, C., Roberts, L.E., Elbert, T., Ross, B. and Wienbruch, C. Tonotopic organization of the sources of human auditory steady-state responses. Hear. Res., 1996, 101: 62–74.
Patuzzi, R.B. and Thomson, S.M. Auditory evoked response test strategies to reduce cost and increase efficiency: the postauricular muscle response revisited. Audiol. Neurootol., 2000, 5: 322–332.
Pelizzone, M., Hari, R., Makela, J.P., Huttunen, J., Ahlfors, S. and Hamalainen, M. Cortical origin of middle-latency auditory evoked responses in man. Neurosci. Lett., 1987, 82: 303–307.
Picton, T.W., Hillyard, S.A., Krausz, H.I. and Galambos, R. Human auditory evoked potentials. I Evaluation of components. Electroencephalogr. Clin. Neurophysiol., 1974, 36: 179–190.
Picton, T.W., Skinner, C.R., Champagne, S.C., Kellett, A.J. and Maiste, A.C. Potentials evoked by the sinusoidal modulation of the amplitude or frequency of a tone. J. Acoust. Soc. Am., 1987, 82: 165–178.
Plourde, G., Stapells, D.R. and Picton, T.W. The human auditory steady-state evoked potentials. Acta Otolaryngol. Suppl. (Stockh), 1991, 491: 153–160.
Rees, A. and Mø ller, A.R. Response of neurons in the inferior colliculus of the rat to AM and FM tones. Hear. Res., 1983, 10: 301–330.
Rei, G. and Fu, B.T. Diagnostic significance of the staggered spondaic word test and 40-Hz auditory event-related potentials. Audiology, 1988, 27: 8–16.
Regan, D. Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine. Elsevier, New York, 1989.
Ribary, U., Ioannides, A.A., Singh, K.D., Hasson, R., Bolton, J.P., Lado, F., Mogilner, A. and Llinas, R. Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc. Natl. Acad. Sci. USA, 1991, 88: 11037–11041.
Rickards, F.W. and Clark, G.M. Steady-state evoked potentials to amplitude-modulated tones. In: R.H. Nodar and C. Barber (Eds.), Evoked Potentials II. Butterworth, Boston, 1984: 163–168.
Roß , B., Borgmann, C., Draganova, R., Roberts, L.E. and Pantev, C. A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. J. Acoust. Soc. Am., 2000, 108: 679–691.
Roß , B., Picton, T.W. and Pantev, C. The onset of the steady-state response reflects temporal integration in the auditory system. Hear. Res., 2002, 165:68–84.
Santarelli, R., Maurizi, M., Conti, G., Ottaviani, F., Paludetti, G. and Pettorossi, V.E. Generation of human auditory steady-state responses (SSRs). II. Addition of responses to individual stimuli. Hear. Res., 1995, 83: 9–18.
Scherg, M. Fundamentals of dipole source potential analysis. In: F. Grandori, M. Hoke, G.L. Romani (Eds.), Advances in Audiology. Volume 6. Auditory Evoked Magnetic Fields and Electric Potentials. Karger, Basel, 1990: 40–69.
Scherg, M., Ille, N., Bornfleth, H. and Berg, P. Advanced tools for digital EEG review: virtual source motages, whole-head mapping, correlation, and phase analysis. J. Clin. Neurophys., 2002, 19(2): 91–112.
Scherg, M. and von Cramon, D. Evoked dipole source potentials of the human auditory cortex. Electroencephalogr. Clin. Neurophysiol., 1986, 65: 344–360.
Scherg, M. and Picton, T.W. Separation and identification of event-related potential components by brain electric source analysis. In: C.H.M. Brunia, G. Mulder and M.N. Verbaten (Eds.), Event-Related Brain Research. Electroencephalogr. Clin. Neurophysiol. Suppl. 42. Elsevier, Amsterdam, 1991:24–37.
Scherg, M., Vajsar, J. and Picton, T.W. A source analysis of the late human auditory evoked potentials. J. Cogn. Neurosci., 1989, 1: 336–355.
Schoonhoven, R., Boden, C.J.R., Verbunt, J.P.A. and de Munck, J.C. A whole-head MEG study of the amplitude modulation following response (AMFR): phase coherence, group delays and dipole source analysis. Paper presented at 17th meeting of the Evoked Response Audiometry Study Group, Vancouver, Canada, July, 2001.
Smith, D.I. and Kraus, N. Intracranial and extracranial recordings of the auditory middle latency response. Electroencephalogr. Clin. Neurophysiol., 1988, 71: 296–303.
Spydell, J.D., Pattee, G. and Goldie, W.D. The 40 Hertz auditory event-related potential: normal values and effects of lesions. Electroencephalogr. Clin. Neurophysiol., 1985, 62: 193–202.
Stapells, D.R., Linden, D., Suffield, J., Hamel, G. and Picton, T.W. Human auditory steady-state potentials. Ear Hear., 1984, 5: 105–113.
Stapells, D.R., Makeig, S. and Galambos, R. Auditory steady-state responses: threshold prediction using phase coherence. Electroencephalogr. Clin. Neurophysiol., 1987, 67: 260–270.
Stapells, D.R., Galambos, R., Costello, J.A. and Makeig, S. Inconsistency of auditory middle latency and steady-state responses in infants. Electroencephalogr. Clin. Neurophysiol., 1988, 71: 289–295.
Starr, A., Picton, T.W., Sininger, Y., Hood, L.J. and Berlin, C.I. Auditory neuropathy. Brain, 1996, 119: 741–753.
Suzuki, T. and Kobayashi, K. An evaluation of 40-Hz event-related potentials in young children. Audiology, 1984, 23: 599–604.
Wood, C.C. and Wolpaw, J.R. Scalp distribution of human auditory evoked potentials. II. Evidence for overlapping sources and involvement of auditory cortex. Electroencephalogr. Clin. Neurophysiol., 1982, 54: 25–38.
Yvert, B., Crouzeix, A., Bertrand, O., Seither-Preisler, A. and Pantev, C. Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. Cerebr. Cortex, 2001, 11: 411–23.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Herdman, A.T., Lins, O., Van Roon, P. et al. Intracerebral Sources of Human Auditory Steady-State Responses. Brain Topogr 15, 69–86 (2002). https://doi.org/10.1023/A:1021470822922
Issue Date:
DOI: https://doi.org/10.1023/A:1021470822922