Abstract
We used magnetoencephalography to examine lateralization and binaural interaction of the middle-latency and late-brainstem components of the auditory evoked response (the MLR and SN10, respectively). Click stimuli were presented either monaurally, or binaurally with left- or right-leading interaural time differences (ITDs). While early MLR components, including the N19 and P30, were larger for monaural stimuli presented contralaterally (by approximately 30 and 36 % in the left and right hemispheres, respectively), later components, including the N40 and P50, were larger ipsilaterally. In contrast, MLRs elicited by binaural clicks with left- or right-leading ITDs did not differ. Depending on filter settings, weak binaural interaction could be observed as early as the P13 but was clearly much larger for later components, beginning at the P30, indicating some degree of binaural linearity up to early stages of cortical processing. The SN10, an obscure late-brainstem component, was observed consistently in individuals and showed linear binaural additivity. The results indicate that while the MLR is lateralized in response to monaural stimuli—and not ITDs—this lateralization reverses from primarily contralateral to primarily ipsilateral as early as 40 ms post stimulus and is never as large as that seen with fMRI.
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Ahonen AI, Hämäläinen MS, Kajola MJ et al (1993) 122-channel squid instrument for investigating the magnetic signals from the human brain. Phys Scr T49A:198–205. doi:10.1088/0031-8949/1993/T49A/033
Alain C, Roye A, Arnott SR (2013) Middle- and long-latency auditory evoked potentials: what are they telling us on central auditory disorders? In: Celesia GG (ed) Handbook of Clinical Neurophysiology, Vol. 10 - Disorders of Peripheral and Central Auditory Processing. Elsevier, Amsterdam, pp 177–199
Atcherson SR, Moore PC (2014) Are chirps better than clicks and tonebursts for evoking middle latency responses? J Am Acad Audiol 25:576–583. doi:10.3766/jaaa.25.6.7
Belliveau LAC, Lyamzin DR, Lesica NA (2014) The neural representation of interaural time differences in gerbils is transformed from midbrain to cortex. J Neurosci 34:16796–16808. doi:10.1523/JNEUROSCI.2432-14.2014
Bohórquez J, Ozdamar O (2008) Generation of the 40-Hz auditory steady-state response (ASSR) explained using convolution. Clin Neurophysiol 119:2598–2607. doi:10.1016/j.clinph.2008.08.002
Brugge JF (2013) Anatomy and physiology of auditory pathways and cortex. In: Celesia GG (ed) Handbook of Clinical Neurophysiology, Vol. 10 - Disorders of Peripheral and Central Auditory Processing. Elsevier, Amsterdam, pp 25–59
Buchner H, Fuchs M, Wischmann H-A et al (1994) Source analysis of median nerve and finger stimulated somatosensory evoked potentials: multichannel simultaneous recording of electric and magnetic fields combined with 3d-MR tomography. Brain Topogr 6:299–310. doi:10.1007/BF01211175
Cacace AT, Satya-Murti S, Wolpaw JR (1990) Human middle-latency auditory evoked potentials: vertex and temporal components. Electroencephalogr Clin Neurophysiol 77:6–18
Celesia GG (1976) Organization of auditory cortical areas in man. Brain 99:403–414. doi:10.1093/brain/99.3.403
Clark VP, Fan S, Hillyard SA (1994) Identification of early visual evoked potential generators by retinotopic and topographic analyses. Hum Brain Mapp 2:170–187. doi:10.1002/hbm.460020306
Davis H, Hirsh SK (1979) A slow brain stem response for low-frequency audiometry. Audiology 18:445–461
Debruyne F (1984) Binaural interaction in early, middle and late auditory evoked responses. Scand Audiol 13:293–296
Dobie RA, Berlin CI (1979) Binaural interaction in brainstem-evoked responses. Arch Otolaryngol 105:391–398
Dobie RA, Norton SJ (1980) Binaural interaction in human auditory evoked potentials. Electroencephalogr Clin Neurophysiol 49:303–313
Fifer RC, Sierra-Irizarry B (1988) Clinical applications of the auditory middle latency response. Am J Otol 9(Suppl):47–56
Gaumond RP, Psaltikidou M (1991) Models for the generation of the binaural difference response. J Acoust Soc Am 89:454–456
Geisler CD, Frishkopf LS, Rosenblith WA (1958) Extracranial responses to acoustic clicks in man. Science 128:1210–1211
Glendenning KK, Baker BN, Hutson KA, Masterton RB (1992) Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSO. J Comp Neurol 319:100–122. doi:10.1002/cne.903190110
Godey B, Schwartz D, de Graaf J et al (2001) Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients. Clin Neurophysiol 112:1850–1859. doi:10.1016/S1388-2457(01)00636-8
Gutschalk A (2014) MEG Auditory Research. In: Supek S, Aine CJ (eds) Magnetoencephalography: from signals to dynamic cortical networks. Springer, Berlin Heidelberg, pp 679–711
Gutschalk A, Steinmann I (2015) Stimulus dependence of contralateral dominance in human auditory cortex. Hum Brain Mapp 36:883–896. doi:10.1002/hbm.22673
Gutschalk A, Mase R, Roth R et al (1999) Deconvolution of 40 Hz steady-state fields reveals two overlapping source activities of the human auditory cortex. Clin Neurophysiol 110:856–868. doi:10.1016/S1388-2457(99)00019-X
Gutschalk A, Brandt T, Bartsch A, Jansen C (2012) Comparison of auditory deficits associated with neglect and auditory cortex lesions. Neuropsychologia 50:926–938. doi:10.1016/j.neuropsychologia.2012.01.032
Hashimoto I (1982) Auditory evoked potentials from the human midbrain: slow brain stem responses. Electroencephalogr Clin Neurophysiol 53:652–657. doi:10.1016/0013-4694(82)90141-9
Hashimoto I, Mashiko T, Yoshikawa K et al (1995) Neuromagnetic measurements of the human primary auditory response. Electroencephalogr Clin Neurophysiol Potentials Sect 96:348–356. doi:10.1016/0168-5597(95)00004-C
Hine J, Debener S (2007) Late auditory evoked potentials asymmetry revisited. Clin Neurophysiol 118:1274–1285. doi:10.1016/j.clinph.2007.03.012
Jacobson GP, Grayson AS (1988) The normal scalp topography of the middle latency auditory evoked potential Pa component following monaural click stimulation. Brain Topogr 1:29–36. doi:10.1007/BF01129337
Jäncke L, Wüstenberg T, Schulze K, Heinze H (2002) Asymmetric hemodynamic responses of the human auditory cortex to monaural and binaural stimulation. Hear Res 170:166–178. doi:10.1016/S0378-5955(02)00488-4
Johnson BW, Hautus MJ (2010) Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 48:2610–2619. doi:10.1016/j.neuropsychologia.2010.05.008
Junius D, Riedel H, Kollmeier B (2007) The influence of externalization and spatial cues on the generation of auditory brainstem responses and middle latency responses. Hear Res 225:91–104. doi:10.1016/j.heares.2006.12.008
Kadoya C, Henry T, Beydoun A et al (1998) Middle latency auditory evoked potentials recorded from human temporal lobes and near the upper brainstem. In: Hashimoto I, Kakigi R (eds) Recent advances in human neurophysiology. Elsevier, Amsterdam, pp 256–264
Kaseda Y, Tobimatsu S, Morioka T, Kato M (1991) Auditory middle-latency responses in patients with localized and non-localized lesions of the central nervous system. J Neurol 238:427–432
Kileny P, Paccioretti D, Wilson AF (1987) Effects of cortical lesions on middle-latency auditory evoked responses (MLR).
Königs L, Gutschalk A (2012) Functional lateralization in auditory cortex under informational masking and in silence. Eur J Neurosci 36:3283–3290. doi:10.1111/j.1460-9568.2012.08240.x
Kraus N, McGee T (1990) Clinical applications of the middle latency response. J Am Acad Audiol 1:130–133
Kraus N, Ozdamar O, Hier D, Stein L (1982) Auditory middle latency responses (MLRs) in patients with cortical lesions.
Krumbholz K, Schönwiesner M, Rübsamen R et al (2005) Hierarchical processing of sound location and motion in the human brainstem and planum temporale. Eur J Neurosci 21:230–238. doi:10.1111/j.1460-9568.2004.03836.x
Kuriki S, Nogai T, Hirata Y (1995) Cortical sources of middle latency responses of auditory evoked magnetic field. Hear Res 92:47–51
Langers DRM, van Dijk P, Backes WH (2005) Lateralization, connectivity and plasticity in the human central auditory system. Neuroimage 28:490–499. doi:10.1016/j.neuroimage.2005.06.024
Levine RA (1981) Binaural interaction in brainstem potentials of human subjects. Ann Neurol 9:384–393. doi:10.1002/ana.410090412
Liégeois-Chauvel C, Musolino A, Badier JM et al (1994) Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. Electroencephalogr Clin Neurophysiol Potentials Sect 92:204–214. doi:10.1016/0168-5597(94)90064-7
Lopes da Silva F (2013) EEG and MEG: relevance to neuroscience. Neuron 80:1112–1128. doi:10.1016/j.neuron.2013.10.017
Magezi DA, Krumbholz K (2010) Evidence for opponent-channel coding of interaural time differences in human auditory cortex. J Neurophysiol 104:1997–2007. doi:10.1152/jn.00424.2009
Mäkelä JPP, Hämäläinen M, Hari R et al (1994) Whole-head mapping of middle-latency auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 92:414–421. doi:10.1016/0168-5597(94)90018-3
McEvoy L, Hari R, Imada T, Sams M (1993) Human auditory cortical mechanisms of sound lateralization: II. Interaural time differences at sound onset. Hear Res 67:98–109. doi:10.1016/0378-5955(93)90237-U
McEvoy L, Mäkelä JP, Hämäläinen M, Hari R (1994) Effect of interaural time differences on middle-latency and late auditory evoked magnetic fields. Hear Res 78:249–257
McLaughlin SA, Higgins NC, Stecker GC (2015) Tuning to binaural cues in human auditory cortex. J Assoc Res Otolaryngol. doi:10.1007/s10162-015-0546-4
McPherson DL, Starr A (1993) Binaural interaction in auditory evoked potentials: brainstem, middle- and long-latency components. Hear Res 66:91–98. doi:10.1016/0378-5955(93)90263-Z
McPherson DL, Tures C, Starr A (1989) Binaural interaction of the auditory brain-stem potentials and middle latency auditory evoked potentials in infants and adults. Electroencephalogr Clin Neurophysiol Potentials Sect 74:124–130. doi:10.1016/0168-5597(89)90017-8
Møller AR, Jannetta PJ (1982) Evoked potentials from the inferior colliculus in man. Electroencephalogr Clin Neurophysiol 53:612–620. doi:10.1016/0013-4694(82)90137-7
Mukamel R, Gelbard H, Arieli A et al (2005) Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309:951–954. doi:10.1126/science.1110913
Musiek FE, Geurkink NA, Weider DJ, Donnelly K (1984) Past, present, and future applications of the auditory middle latency response. Laryngoscope 94:1545–1553
Ozdamar O, Kraus N (1983) Auditory middle-latency responses in humans. Audiology 22:34–49
Ozdamar O, Bohórquez J (2008) Suppression of the P(b) (P(1)) component of the auditory middle latency response with contralateral masking. Clin Neurophysiol 119:1870–1880. doi:10.1016/j.clinph.2008.03.023
Özdamar Ö, Kraus N, Curry F (1982) Auditory brain stem and middle latency responses in a patient with cortical deafness. Electroencephalogr Clin Neurophysiol 53:224–230. doi:10.1016/0013-4694(82)90027-X
Palomäki KJ, Tiitinen H, Mäkinen V et al (2005) Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques. Brain Res Cogn Brain Res 24:364–379. doi:10.1016/j.cogbrainres.2005.02.013
Pantev C, Lütkenhöner B, Hoke M, Lehnertz K (1986) Comparison between simultaneously recorded auditory-evoked magnetic fields and potentials elicited by ipsilateral, contralateral and binaural tone burst stimulation. Audiology 25:54–61
Parkkonen L, Fujiki N, Mäkelä JP (2009) Sources of auditory brainstem responses revisited: contribution by magnetoencephalography. Hum Brain Mapp 30:1772–1782. doi:10.1002/hbm.20788
Peters JF, Mendel MI (1974) Early components of the averaged electroencephalic response to monaural and binaural stimulation. Int J Audiol 13:195–204. doi:10.3109/00206097409071677
Phillips DP, Gates GR (1982) Representation of the two ears in the auditory cortex: a re-examination. Int J Neurosci 16:41–46
Picton TW, Hillyard SA, Krausz HI, Galambos R (1974) Human auditory evoked potentials. I: Evaluation of components. Electroencephalogr Clin Neurophysiol 36:179–190. doi:10.1016/0013-4694(74)90155-2
Plourde G (2006) Auditory evoked potentials. Best Pract Res Clin Anaesthesiol 20:129–139. doi:10.1016/j.bpa.2005.07.012
Polyakov A, Pratt H (1995) Three-channel Lissajous’ trajectory of the binaural interaction components of human auditory middle-latency evoked potentials. Hear Res 82:205–215. doi:10.1016/0378-5955(94)00178-S
Pratt H (2013) Sensory ERP components. In: Luck SJ, Kappenman ES (eds) The Oxford handbook of event-related potential components. Oxford University Press, Oxford, pp 89–114
Reser DHH, Fishman YI, Arezzo JC, Steinschneider M (2000) Binaural interactions in primary auditory cortex of the awake macaque. Cereb Cortex 10:574–584. doi:10.1093/cercor/10.6.574
Riedel H, Kollmeier B (2002) Comparison of binaural auditory brainstem responses and the binaural difference potential evoked by chirps and clicks. Hear Res 169:85–96. doi:10.1016/S0378-5955(02)00342-8
Riedel H, Kollmeier B (2006) Interaural delay-dependent changes in the binaural difference potential of the human auditory brain stem response. Hear Res 218:5–19. doi:10.1016/j.heares.2006.03.018
Rodieck RW (1979) Visual pathways. Annu Rev Neurosci 2:193–225
Ross B, Herdman AT, Pantev C (2005) Right hemispheric laterality of human 40 Hz auditory steady-state responses. Cereb Cortex 15:2029–2039. doi:10.1093/cercor/bhi078
Rupp A, Gutschalk A, Hack S, Scherg M (2002a) Temporal resolution of the human primary auditory cortex in gap detection. Neuroreport 13:2203–2207. doi:10.1097/01.wnr.0000045007.30898.39
Rupp A, Uppenkamp S, Gutschalk A et al (2002b) The representation of peripheral neural activity in the middle-latency evoked field of primary auditory cortex in humans. Hear Res 174:19–31. doi:10.1016/S0378-5955(02)00614-7
Salminen NH, May PJC, Alku P, Tiitinen H (2009) A population rate code of auditory space in the human cortex. PLoS One 4:e7600. doi:10.1371/journal.pone.0007600
Salminen NH, Tiitinen H, Yrttiaho S, May PJC (2010) The neural code for interaural time difference in human auditory cortex. J Acoust Soc Am 127:EL60–EL65. doi:10.1121/1.3290744
Salminen NH, Tiitinen H, May PJC (2012) Auditory spatial processing in the human cortex. Neuroscientist 18:602–612. doi:10.1177/1073858411434209
Scheffler K, Bilecen D, Schmid N et al (1998) Auditory cortical responses in hearing subjects and unilateral deaf patients as detected by functional magnetic resonance imaging. Cereb Cortex 8:156–163. doi:10.1093/cercor/8.2.156
Scherg M, Von Cramon D (1986) Evoked dipole source potentials of the human auditory cortex. Electroencephalogr Clin Neurophysiol 65:344–360
Shaw ME, Hämäläinen MS, Gutschalk A (2013) How anatomical asymmetry of human auditory cortex can lead to a rightward bias in auditory evoked fields. Neuroimage 74:22–29. doi:10.1016/j.neuroimage.2013.02.002
Singh KD (2012) Which “neural activity” do you mean? fMRI, MEG, oscillations and neurotransmitters. Neuroimage 62:1121–1130. doi:10.1016/j.neuroimage.2012.01.028
Stecker GC, McLaughlin SA, Higgins NC (2015) Monaural and binaural contributions to interaural-level-difference sensitivity in human auditory cortex. Neuroimage 120:456–466. doi:10.1016/j.neuroimage.2015.07.007
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 (New York, NY 1991) 18:610–625. doi:10.1093/cercor/bhm094
Tawfik S, Musiek FE (1991) SN10 auditory evoked potential revisited. Am J Otol 12:179–183
Thompson SK, von Kriegstein K, Deane-Pratt A et al (2006) Representation of interaural time delay in the human auditory midbrain. Nat Neurosci 9:1096–1098. doi:10.1038/nn1755
van Olphen AF, Rodenburg M, Verwey C (1978) Distribution of brain stem responses to acoustic stimuli over the human scalp. Audiology 17:511–518
von Kriegstein K, Griffiths TD, Thompson SK, McAlpine D (2008) Responses to interaural time delay in human cortex. J Neurophysiol 100:2712–2718. doi:10.1152/jn.90210.2008
Vonderschen K, Wagner H (2014) Detecting interaural time differences and remodeling their representation. Trends Neurosci 37:289–300. doi:10.1016/j.tins.2014.03.002
Wall PD, Dubner R (1972) Somatosensory pathways. Annu Rev Physiol 34:315–336. doi:10.1146/annurev.ph.34.030172.001531
Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–446. doi:10.1038/nature02116
Woldorff MG, Tempelmann C, Fell J et al (1999) Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum Brain Mapp 7:49–66. doi:10.1002/(SICI)1097-0193(1999)7:1<49::AID-HBM5>3.0.CO;2-J
Woods DL, Clayworth CC (1985) Click spatial position influences middle latency auditory evoked potentials (MAEPs) in humans. Electroencephalogr Clin Neurophysiol 60:122–129. doi:10.1016/0013-4694(85)90018-5
Woods DL, Clayworth CC, Knight RT et al (1987) Generators of middle- and long-latency auditory evoked potentials: implications from studies of patients with bitemporal lesions. Electroencephalogr Clin Neurophysiol 68:132–148
Woods DL, Herron TJ, Cate AD et al (2010) Functional properties of human auditory cortical fields. Front Syst Neurosci 4:155. doi:10.3389/fnsys.2010.00155
Wrege K, Starr A (1981) Binaural interaction in human auditory brainstem evoked potentials. Arch Neurol 38:572–580
Yao JD, Bremen P, Middlebrooks JC (2015) Transformation of spatial sensitivity along the ascending auditory pathway. J Neurophysiol 113:3098–3111. doi:10.1152/jn.01029.2014
Yvert B, Crouzeix A, Bertrand O et al (2001) Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. Cereb Cortex 11:411–423. doi:10.1093/cercor/11.5.411
Yvert B, Fischer C, Guénot M et al (2002) Simultaneous intracerebral EEG recordings of early auditory thalamic and cortical activity in human. Eur J Neurosci 16:1146–1150. doi:10.1046/j.1460-9568.2002.02162.x
Yvert B, Fischer C, Bertrand O, Pernier J (2005) Localization of human supratemporal auditory areas from intracerebral auditory evoked potentials using distributed source models. Neuroimage 28:140–153. doi:10.1016/j.neuroimage.2005.05.056
Acknowledgments
The authors would like to thank Barbara Burghardt and Esther Tauberschmidt for assistance with the data collection as well as two anonymous reviewers for helpful comments. This work was supported by the German Federal Ministry of Education and Research (BMBF) grant number 01EV0712 to AG.
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Dykstra, A.R., Burchard, D., Starzynski, C. et al. Lateralization and Binaural Interaction of Middle-Latency and Late-Brainstem Components of the Auditory Evoked Response. JARO 17, 357–370 (2016). https://doi.org/10.1007/s10162-016-0572-x
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DOI: https://doi.org/10.1007/s10162-016-0572-x