Abstract
Processing of acoustic space in the human auditory system implicates the interaction of the left and right hemispheres of the brain. In this study, we investigated the influence of the position and motion direction of sound stimuli on the amplitude and latency of N1, P2, MMN, and P3a components of auditory evoked potentials in the left and right brain hemispheres. The data suggest that functional asymmetry of the N1P2 complex and difference waveforms can be described as weak contralateral dominance. Deviants moving from the lateral positions evoked later P3a components than those moving from the midline, which is consistent with the concept of higher localization accuracy in the frontal part of the acoustic space. The motion direction affected the MMN and P3a latency: the centrifugal deviants produced earlier MMN and P3a responses than the centripetal deviants. This could result from a stronger orienting reaction caused by stimuli moving from the center towards the periphery as compared with the opposite direction.
Similar content being viewed by others
REFERENCES
Kandel, E.R., The neurobiology of behavior, in Principles of Neural Sciences, Kandel, E.R., Schwartz, J.H., and Jessel, T.M., Eds., New York: McGraw-Hill, 2000, 4th ed.
Vulliemoz, S., Raineteau, O., and Jabaudon, D., Reaching beyond the midline: why are human brains cross wired? Lancet Neurol., 2005, vol. 4, no. 2, p. 87.
Phillips, D.P. and Brugge, J.F., Progress in neurophysiology of sound localization, Annu. Rev. Psychol., 1985, vol. 36, p. 245.
McAlpine, D., Jiang, D., and Palmer, A.R., A neural code for low frequency sound localization in mammals, Nat. Neurosci., 2001, vol. 4, no. 4, p. 396.
Hart, H.C., Palmer, A.R., and Hall, D.A., Different areas of human non-primary auditory cortex are activated by sounds with spatial and nonspatial properties, Hum. Brain Mapp., 2004, vol. 21, no. 3, p. 178.
Spierer, L., Bellmann-Thiran, A., Maeder, Ph., et al., Hemispheric competence for auditory spatial representation, Brain, 2009, vol. 132, no. 7, p. 1953.
Fujiki, N., Riederer, K.A.J., Jousmäki, V., et al., Human cortical representation of virtual auditory space: differences between sound azimuth and elevation, Eur. J. Neurosci., 2002, vol. 16, no. 11, p. 2207.
Palomäki, K., Alku, P., Mäkinen, V., et al., Sound localization in the human brain: neuromagnetic observations, Neuroreport, 2000, vol. 11, no. 7, p. 1535.
Palomäki, K.J., Tiitinen, H., Mäkinen, V., et al., Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques, Cognit. Brain Res., 2005, vol. 24, no. 3, p. 364.
Krumbholz, K., Schonwiesner, M., von Cramon, D.Y., et al., Representation of interaural temporal information from left and right auditory space in the human planum temporale and inferior parietal lobe, Cereb. Cortex, 2005, vol. 15, no. 3, p. 317.
Getzmann, S., Effect of auditory motion velocity on reaction time and cortical processes, Neuropsychologia, 2009, vol. 47, no. 12, p. 2625.
Getzmann, S., Auditory motion perception: onset position and motion direction are encoded in discrete processing stages, Eur. J. Neurosci., 2011, vol. 33, no. 7, p. 1339.
Tanaka, H., Hachisuka, K., and Ogata, H., Sound lateralization in patients with left or right cerebral hemispheric lesions: relation with unilateral visuospatial neglect, J. Neurol. Neurosurg. Psychiatry, 1999, vol. 67, no. 4, p. 481.
Zatorre, R.J., Mondor, T.A., and Evans, A.C., Auditory attention to space and frequency activates similar cerebral systems, NeuroImage, 1999, vol. 10, no. 5, p. 544.
Brunetti, M., Belardinelli, P., Caulo, M., et al., Human brain activation during passive listening to sounds from different locations: an fMRI and MEG study, Hum. Brain Mapp., 2005, vol. 26, no. 4, p. 251.
Tiitinen, H., Salminen, N.H., Palomaki, K.J., et al., Neuromagnetic recordings reveal the temporal dynamics of auditory spatial processing in the human cortex, Neurosci. Lett., 2006, vol. 396, no. 1, p. 17.
Baumgart, F., Gaschler-Markefski, B., Woldorff, M.G., et al., A movement-sensitive area in auditory cortex, Nature, 1999, vol. 400, no. 6746, p. 724.
Griffiths, T.D., Rees, G., Rees, A., et al., Right parietal cortex is involved in the perception of sound movement in humans, Nat. Neurosci., 1998, vol. 1, no. 1, p. 74.
Krumbholz, K., Hewson-Stoate, N., and Schönwiesner, M., Cortical response to auditory motion suggests an asymmetry in the reliance on inter-hemispheric connections between the left and right auditory cortices, J. Neurophysiol., 2007, vol. 97, no. 2, p. 1649.
Briley, P.M., Kitterick, P.T., and Summerfield, A.Q., Evidence for opponent process analysis of sound source location in humans, J. Assoc. Res. Otolaryngol., 2013, vol. 14, no. 1, p. 83.
Ahveninen, J., Kopco, N., and Jääskeläinen, I.P., Psychophysics and neuronal bases of sound localization in humans, Hear. Res., 2014, vol. 307, p. 86.
Mesulam, M.M., Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events, Philos. Trans. R. Soc., B, 1999, vol. 354, no. 1387, p. 1325.
Teshiba, T.M., Ling, J., Ruhl, D.A., et al., Evoked and intrinsic asymmetries during auditory attention: implications for the contralateral and neglect models of functioning, Cereb. Cortex, 2013, vol. 23, no. 3, p. 560.
Deouell, L.Y., Bentin, S., and Giard, M.H., Mismatch negativity in dichotic listening: Evidence for interhemispheric differences and multiple generators, Psychophysiology, 1998, vol. 35, no. 4, p. 355.
Kaiser, J., Lutzenberger, W., Preissl, H., et al., Right-hemisphere dominance for the processing of sound-source lateralization, J. Neurosci., 2000, vol. 20, no. 17, p. 6631.
Schonwiesner, M., Krumbholz, K., Rubsamen, R., et al., Hemispheric asymmetry for auditory processing in the human auditory brainstem, thalamus, and cortex, Cereb. Cortex, 2007, vol. 17, no. 2, p. 492.
Näätänen, R., The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function, Behav. Brain Sci., 1990, vol. 13, no. 2, p. 201.
Kaiser, J. and Lutzenberger, W., Location changes enhance hemispheric asymmetry of magnetic fields evoked by lateralized sounds in humans, Neurosci. Lett., 2001, vol. 314, nos. 1–2, p. 17.
Näätänen, R. Paavilainen, P., Rinne, T., et al., The mismatch negativity (MMN) in basic research of central auditory processing: a review, Clin. Neurophysiol., 2007, vol. 118, no. 12, p. 2544.
Nager, W., Kohlmetz, C., Joppich, G., et al., Tracking of multiple sound sources defined by interaural time differences: brain potential evidence in humans, Neurosci. Lett., 2003, vol. 344, no. 3, p. 181.
Richter, N., Schröger, E., and Rübsamen, R., Hemispheric specialization during discrimination of sound sources reflected by MMN, Neuropsychologia, 2009, vol. 47, no. 12, p. 2652.
Takegata, R., Huotilainen, M., Rinne, T., et al., Changes in acoustic features and their conjunctions are processed by separate neuronal populations, Neuroreport, 2001, vol. 12, no. 3, p. 525.
Tata, M.S. and Ward, L.M., Early phase of spatial mismatch negativity is localized to a posterior “where” auditory pathway, Exp. Brain Res., 2005, vol. 167, no. 3, p. 481.
Vaitulevich, S.F. and Shestopalova, L.B., Interhemisphere asymmetry of auditory evoked potentials in humans and mismatch negativity during sound source localization, Neurosci. Behav. Physiol., 2010, vol. 40, no. 6, p. 629.
Vaitulevich, S.F., Petropavlovskaya, E.A., Shestopalova, L.B., et al., Interhemispheric asymmetry of the total activity of the human brain in the localization of the sound source, Sens. Sist., 2015, vol. 29, no. 2, p. 148.
Altman, J.A., Vaitulevich, S.Ph., Shestopalova, L.B., et al., How does mismatch negativity reflect auditory motion? Hear. Res., 2010, vol. 268, nos. 1–2, p. 194.
Shestopalova, L.B., Petropavlovskaya, E.A., Vaitulevich, S.F., et al., Topography of activity evoked in the human brain during discrimination of moving sound stimuli, Neurosci. Behav. Physiol., 2017, vol. 47, no. 1, p. 83.
Shestopalova, L.B., Petropavlovskaia, E.A., Vaitulevich, S.Ph., et al., Hemispheric asymmetry of ERPs and MMNs evoked by slow, fast and abrupt auditory motion, Neuropsychologia, 2016, vol. 91, p. 465.
Magezi, D.A. and Krumbholz, K., Evidence for opponent-channel coding of interaural time differences in human auditory cortex, J. Neurophysiol., 2010, vol. 104, no. 4, p. 1997.
Petropavlovskaya, E.A., Shestopalova, L.B., and Vaitulevich, S.F., Predictive ability of the auditory system during gradual and abrupt movements of low-intensity sound images, Neurosci. Behav. Physiol., 2012, vol. 42, no. 8, p. 911.
Delorme, A., Sejnowski, T., and Makeig, S., Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis, NeuroImage, 2007, vol. 34, no. 4, p. 1443.
Barcelo, F., Escera, C., Corral, M.J., et al., Task switching and novelty processing activate a common neural network for cognitive control, J. Cognit. Neu-rosci., 2006, vol. 18, no. 10, p. 1734.
Friedman, D., Cycowicz, Y.M., and Gaeta, H., The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty, Neurosci. Biobehav. Res., 2001, vol. 25, no. 4, p. 355.
Rinne, T., Särkkä, A., Degerman, A., et al., Two separate mechanisms underlie auditory change detection and involuntary control of attention, Brain Res., 2006, vol. 1077, no. 1, p. 135.
Horváth, J. and Winkler, I., Distraction in a continuous-stimulation detection task, Biol. Psychol., 2010, vol. 83, no. 3, p. 229.
Al’tman, Ya.A., Lokalizatsiya dvizhushchegosya istochnika zvuka (Localization of Moving Sound Source), Leningrad: Nauka, 1983.
Al’tman, Ya.A., Prostranstvennyi slukh (Spatial Hearing), St. Petersburg: Inst. Fiziol. im. I.P. Pavlova, Ross. Akad. Nauk, 2011.
Coull, J.T., Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology, Prog. Neurobiol., 1998, vol. 55, p. 343.
Polich, J., Updating P300: an integrative theory of P3a and P3b, Clin. Neurophysiol., 2007, vol. 118, no. 10, p. 2128.
Ball, K. and Sekuler, R., Human vision favors centrifugal motion, Perception, 1980, vol. 9, no. 3, p. 317.
Funding
This study was supported by the Basic Research Program for State Academies for 2013–2020 (GP-14, section 63.3).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest. The authors declare no explicit and potential conflicts of interest associated with the publication of this article.
Statement of compliance with standards of research involving humans as subjects. All studies were conducted in accordance with the principles of biomedical ethics set out in the 1964 Helsinki Declaration and its subsequent amendments and approved by the Ethics Committee of the St. Petersburg State University (Saint-Petersburg). Each study participant provided a voluntary written informed consent signed after explanations of potential risks and benefits as well as the nature of the forthcoming investigations.
Additional information
Translated by M. Batrukova
Rights and permissions
About this article
Cite this article
Petropavlovskaia, E.A., Kanakhina, L.A. & Shestopalova, L.B. Effect of Motion Trajectory on the Lateralization of Auditory Evoked Responses. Hum Physiol 46, 351–365 (2020). https://doi.org/10.1134/S0362119720020127
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0362119720020127