Abstract
How does a listener perceive the auditory world and make sense from the myriad of concurrent sounds in the noisy and complex soundscape impinging our ears as a continuous flow? A major emerging view in cognitive auditory neuroscience is that the auditory system implements a pervasive mechanism by which dynamic auditory input is modeled into neural traces of regularities that allow the system to derive perceptual auditory objects. A large number of studies that used auditory sequences of various statistical complexities and that were performed with a range of neuroscience methods (e.g., neuro-imaging, electroencephalography and auditory evoked potentials, single neuron recordings) together have shown that regularity encoding and deviance detection is a key property of the auditory cortex. Furthermore, recordings in the inferior colliculus (IC) and the auditory thalamus of experimental animals have disclosed stimulus-specific adaptation (SSA) at these levels of the auditory pathway, challenging the corticocentric view of regularity encoding and deviance detection. Together with recent experiments using oddball sequences to measure early auditory evoked potentials, such as the middle latency response (MLR) and particularly the frequency-following response (FFR), those studies support the emerging view that regularity encoding and deviance detection are a key functional properties of the entire auditory system from at least the IC to high-order auditory cortical regions, and that the subcortical auditory pathway can implement certain forms of “primitive intelligence”, thereby contributing to auditory cognition.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aghamolaei, M., Zarnowiec, K., Grimm, S., & Escera, C. (2016). Functional dissociations between regularity encoding and deviance detection along the auditory hierarchy. European Journal of Neuroscience, 43(4), 529–535.
Ahveninen, J., Huang, S., Nummenmaa, A., Belliveau, J. W., et al. (2013). Evidence for distinct human auditory cortex regions for sound location versus identity processing. Nature Communications, 4, 2585. Doi:10.1038/ncomms3585
Alho, K., Grimm, S., Mateo-León, S., Costa-Faidella, J., & Escera, C. (2012). Early processing of pitch in the human auditory system. European Journal of Neuroscience, 36, 2972–2978.
Althen, H., Grimm, S., & Escera, C. (2011). Fast detection of unexpected sound intensity decrements as revealed by human evoked potentials. PLoS ONE, 6(12), e28522. Doi:10.1371/journal.pone.0028522
Anderson, L. A., & Malmierca, M. S. (2013). The effect of auditory cortical deactivation on stimulus-specific adaptation in the inferior colliculus of the rat. European Journal of Neuroscience, 37, 52–62.
Anderson, S., White-Schwoch, T., Parbery-Clark, A., & Kraus, N. (2013). Reversal of age-related neural timing delays with training. Proceedings of the National Academy of Sciences of the USA, 110(11), 4357–4362.
Antunes, F. M., & Malmierca, M. S. (2011). Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body. The Journal of Neuroscience, 31, 17306–17316.
Antunes, F. M., Nelken, I., Covey, E., & Malmierca, M. S. (2010). Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS ONE, 5, e14071.
Ayala, Y. A., & Malmierca, M. S. (2015). Cholinergic modulation of stimulus-specific adaptation in the inferior colliculus. The Journal of Neuroscience, 35(35), 12261–12272.
Ayala, Y. A., Pérez-González, D., Duque, D., Nelken, I., & Malmierca, M. S. (2012). Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Frontiers in Neural Circuits, 6, 119. Doi:10.3389/fncir.2012.00119
Bajo, V. M., Nodal, F. R., Moore, D. R., & King, A. J. (2010). The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nature Neuroscience, 13(2), 253–260.
Bellier, L., Bouchet, P., Jeanvoine, A., Valentin, O., et al. (2015). Topographic recordings of auditory evoked potentials to speech: Subcortical and cortical responses. Psychophysiology, 52(4), 549–594.
Bendixen, A., Prinz, W., Horváth, J., Trujillo-Barreto, N. J., & Schröger, E. (2008). Rapid extraction of auditory feature contingencies. NeuroImage, 41(3), 1111–1119.
Bidelman, G. M. (2015). Towards an optimal paradigm for simultaneously recording cortical and brainstem auditory evoked potentials. The Journal of Neuroscience Methods, 15(241), 94–100.
Bregman, A. (1990). Auditory scene analysis. The perceptual organization of sound. Cambridge, MA: MIT Press.
Cacciaglia, R., Escera, C., Slabu, L. S., Grimm, S., et al. (2015). Involvement of the human midbrain and thalamus in auditory deviance detection. Neuropsychologia, 68, 51–58.
Chandrasekaran, B., Hornickel, J., Skoe, E., Nicol, T., & Kraus, N. (2009). Context-dependent encoding in the human auditory brainstem relates to hearing speech in noise: Implications for developmental dyslexia. Neuron, 64(3), 311–319.
Chandrasekaran, B., & Kraus, N. (2010). The scalp-recorded brainstem response to speech: Neural origins and plasticity. Psychophysiology, 47, 236–246.
Chandrasekaran, B., Kraus, N., & Wong, P. C. (2012). Human inferior colliculus activity relates to individual differences in spoken language learning. Journal of Neurophysiology, 107(5), 1325–1336.
Chandrasekaran, B., Skoe, E., & Kraus, N. (2014). An integrative model of subcortical auditory plasticity. Brain Topography, 27(4), 539–552.
Chen, I. W., Helmchen, F., & Lütcke, H. (2015). Specific early and late oddball-evoked responses in excitatory and inhibitory neurons of mouse auditory cortex. The Journal of Neuroscience, 35(36), 12560–12573.
Coffey, E. B. J., Herholz, S. C., Cepesiuk, A. M. P., Baillet, S., & Zatorre, R. J. (2016). Cortical contributions to the auditory frequency-following response revealed by MEG. Nature Communications, 7, 11070. Doi:10.1038/ncomms11070
Cornella, M., Leung, S., Grimm, S., & Escera, C. (2012). Detection of simple and pattern regularity violations occurs at different levels of the auditory hierarchy. PLoS ONE, 7(8), e43604.
Cornella, M., Leung, S., Grimm, S., & Escera, C. (2013). Regularity encoding and deviance detection of frequency modulated sweeps: Human middle- and long-latency auditory evoked potentials. Psychophysiology, 50, 1275–1281.
Costa-Faidella, J., Baldeweg, T., Grimm, S., & Escera, C. (2011a). Interactions between “what” and “when” in the auditory system: Temporal predictability enhances repetition suppression. The Journal of Neuroscience, 31, 18590–18597.
Costa-Faidella, J., Grimm, S., Slabu, L., Díaz-Santaella, F., & Escera, C. (2011b). Multiple time scales of adaptation in the auditory system as revealed by human evoked potentials. Psychophysiology, 48, 774–783.
Davis, R. L., & Britt, R. H. (1984). Analysis of the frequency following response in the cat. Hearing Research, 15(1), 29–37.
Deouell, L. Y. (2007). The frontal generator of the mismatch negativity revisited. Journal of Psychophysiology, 21, 188–203.
Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proceeding of the National Academy of Sciences of the U S A, 93(24), 13494–13499.
Escera, C., Alho, K., Winkler, I., & Näätänen, R. (1998). Neural mechanisms of involuntary attention to acoustic novelty and change. Journal of Cognitive Neuroscience, 10, 590–604.
Escera, C., & Corral, M. J. (2007). Role of mismatch negativity and novelty-P3 in involuntary auditory attention. Journal of Psychophysiology, 21, 251–264.
Escera, C., Leung, S., & Grimm, S. (2014). Deviance detection based on regularity encoding along the auditory hierarchy: Electrophysiological evidence in humans. Brain Topography, 27(4), 527–538.
Escera, C., & Malmierca, M. S. (2014). The auditory novelty system: An attempt to integrate human and animal research. Psychophysiology, 51, 111–123.
Farley, B. J., Quirk, M. C., Doherty, J. J., & Christian, E. P. (2010). Stimulus-specific adaptation in auditory cortex is an NMDA-independent process distinct from the sensory novelty encoded by the mismatch negativity. The Journal of Neuroscience, 30, 16475–16484.
Ford, J. M., & Hillyard, S. A. (1981). Event-related potentials (ERPs) to interruptions of a steady rhythm. Psychophysiology, 18(3), 322–330.
Friston, K. (2005). A theory of cortical responses. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 360(1456), 815–836.
Friston, K., Kilner, J., & Harrison, L. (2006). A free energy principle for the brain. Journal of Physiololgy (Paris), 100(1–3), 70–87.
Gorina-Careta, N., Zarnowiec, K., Costa-Faidella, C., & Escera, C. (2016). Timing predictability enhances regularity encoding in the human subcortical auditory pathway. Scientific Reports, 6, 37405. doi:10.1038/srep37405.
Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: Neural models of stimulus-specific effects. Trends in Cognitive Sciences, 10, 14–23.
Grimm, S., & Escera, C. (2012). Auditory deviance detection revisited: Evidence for a hierarchical novelty system. International Journal of Psychophysiology, 85, 88–92.
Grimm, S., Escera, C., & Nelken, I. (2016). Early indices of deviance detection in humans and animal models. Biological Psychology, 116, 23–27.
Grimm, S., Escera, C., Slabu, L. M., & Costa-Faidella, J. (2011). Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain. Psychophysiology, 48, 377–384.
Grimm, S., Recasens, M., Althen, H., & Escera, C. (2012). Ultrafast tracking of sound location changes as revealed by human auditory evoked potentials. Biological Psychology, 89, 232–239.
Haenschel, C., Vernon, D. J., Dwivedi, P., Gruzelier, J. H., & Baldeweg, T. (2005). Event-related brain potential correlates of human auditory sensory memory-trace formation. Journal of Neuroscience, 25, 10494–10501.
Jeng, F. C., Chung, H. K., Lin, C. D., Dickman, B., & Hu, J. (2011). Exponential modeling of human frequency-following responses to voice pitch. International Journal of Audiology, 50(9), 582–593.
Joris, P. X., Schreiner, C. E., & Rees, A. (2004). Neural processing of amplitude-modulated sounds. Physiological Review, 84(2), 541–577.
Kraus, N., McGee, T., Littman, T., Nicol, T., & King, C. (1994). Nonprimary auditory thalamic representation of acoustic change. Journal of Neurophysiology, 72, 1270–1277.
Krizman, J., Marian, V., Shook, A., Skoe, E., & Kraus, N. (2012). Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages. Proceedings of the National Academy of Sciences of the U S A, 109(20), 7877–7881.
Leung, S., Recasens, M., Grimm, S., & Escera, C. (2013). Electrophysiological index of acoustic temporal regularity violation in the middle latency range. Clinical Neurophysiology, 124, 2397–2405.
Malmierca, M. S., Anderson, L. A., & Antunes, F. M. (2015). The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: A potential neuronal correlate for predictive coding. Frontiers in Systems Neuroscience, 9, 19. Doi:10.3389/fnsys.2015.00019
Malmierca, M. S., Cristaudo, S., Perez-Gonzalez, D., & Covey, E. (2009). Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. The Journal of Neuroscience, 29, 5483–5493.
Møller, A. R., Jannetta, P. J., & Sekhar, L. N. (1988). Contributions from the auditory nerve to the brain-stem auditory evoked potentials (BAEPs): Results of intracranial recording in man. Electroencephalography and Clinical Neurophysiology, 71, 198–211.
Näätänen, R., Astikainen, P., Ruusuvirta, T., & Huotilainen, M. (2010). Automatic auditory intelligence: An expression of the sensory-cognitive core of cognitive processes. Brain Research Reviews, 64(1), 123–136.
Näätänen, R., Paavilainen, P., Rinne, T., & Alho, K. (2007). The mismatch negativity (MMN) in basic research of central auditory processing: A review. Clinical Neurophysiology, 118, 2544–2590.
Näätänen, R., Tervaniemi, M., Sussman, E., Paavilainen, P., & Winkler, I. (2001). “Primitive intelligence” in the auditory cortex. Trends in Neurosciences, 24, 283–288.
Näätänen, R., & Winkler, I. (1999). The concept of auditory stimulus representation in cognitive neuroscience. Psychological Bulletin, 6, 826–859.
Nelken, I. (2014). Stimulus-specific adaptation and deviance detection in the auditory system: Experiments and models. Biological Cybernetics, 108, 655–663.
Nelken, I., & Ulanovsky, N. (2007). Mismatch negativity and stimulus-specific adaptation in animal models. Journal of Psychophysiology, 21, 214–223.
Opitz, B., Mecklinger, A., Von Cramon, D. Y., & Kruggel, F. (1999). Combining electrophysiological and hemodynamic measures of the auditory oddball. Psychophysiology, 36(1), 142–147.
Paavilainen, P. (2013). The mismatch-negativity (MMN) component of the auditory event-related potential to violations of abstract regularities: A review. International Journal of Psychophysiology, 88, 109–123.
Parbery-Clark, A., Strait, D. L., & Kraus, N. (2011). Context-dependent encoding in the auditory brainstem subserves enhanced speech-in-noise perception in musicians. Neuropsychologia, 49(12), 3338–3345.
Parkkonen, L., Fujiki, N., & Mäkelä, J. P. (2009). Sources of auditory brainstem responses revisited: Contribution by magnetoencephalography. Human Brain Mapping, 30(6), 1772–1782.
Parvizi, J. (2009). Corticocentric myopia: Old bias in new cognitive sciences. Trends in Cognitive Sciences, 13(8), 354–359.
Pérez-González, D., Covey, E., & Malmierca, M. S. (2005). Novelty detector neurons in the mammalian auditory midbrain. European Journal of Neuroscience, 22, 2879–2885.
Pérez-González, D., Hernandez, O., Covey, E., & Malmierca, M. S. (2012). GABA(A)-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS ONE, 7, e34297.
Picton, T. W. (2011). Human auditory evoked potentials. San Diego: Plural Publishing.
Recasens, M., Grimm, S., Capilla, A., Nowak, R., & Escera, C. (2014). Two sequential processes of change detection in hierarchically ordered areas of the human auditory cortex. Cerebral Cortex, 24, 143–153.
Recasens, M., Leung, S., Grimm, S., Nowak, R., & Escera, C. (2015). Repetition suppression and repetition enhancement underlie auditory memory-trace formation in the human brain: An MEG study. NeuroImage, 108, 75–86.
Riecke, L., Formisano, E., Herrmann, C. S., & Sack, A. T. (2015). 4-Hz Transcranial alternating current stimulation phase modulates hearing. Brain Stimulation, 8(4), 777–783.
Ruhnau, P., Herrmann, B., & Schröger, E. (2012). Finding the right control: The mismatch negativity under investigation. Clinical Neurophysiology, 123, 507–512.
Sabri, M., Kareken, D. A., Dzemidzic, M., Lowe, M. J., & Melara, R. D. (2004). Neural correlates of auditory sensory memory and automatic change detection. NeuroImage, 21(1), 69–74.
Schaefer, J., Zarnowiec, K., SanMiguel, I., Malmierca, M. S., & Escera, C. (2015). Predicting complex acoustic contingencies in the human auditory brainstem. In A. Widmann, J. Steinberg, A. Bendixen, A. D. Friederici, et al. (Eds.), Error Signals from the Brain: 7th Mismatch Negativity Conference (pp. 61–62). Leipzig: University of Leipzig Press.
Schröger, E., & Wolff, C. (1996). Mismatch response to changes in sound location. NeuroReport, 7, 3005–3008.
Shiga, T., Althen, H., Cornella, M., Zarnowiec, K., et al. (2015). Deviance-related responses along the auditory hierarchy: Combined FFR. MLR and MMN evidence. PLOS ONE, 10(9), e0136794. Doi:10.1371/journal.pone.0136794
Skoe, E., & Chandrasekaran, B. (2014). The layering of auditory experiences in driving experience-dependent subcortical plasticity. Hearing Research, 311, 36–48.
Skoe, E., Chandrasekaran, B., Spitzer, E. R., Wong, P. C., & Kraus, N. (2014). Human brainstem plasticity: The interaction of stimulus probability and auditory learning. Neurobiology of Learning and Memory, 109, 82–93.
Skoe, E., & Kraus, N. (2010a). Auditory brainstem response to complex sounds: A tutorial. Ear and Hearing, 31, 302–324.
Skoe, E., & Kraus, N. (2010b). Hearing it again and again: On-line subcortical plasticity in humans. PLoS ONE, 5(10), e13645. Doi:10.1371/journal.pone.0013645
Skoe, E., Krizman, J., Spitzer, E., & Kraus, N. (2013). The auditory brainstem is a barometer of rapid auditory learning. Neuroscience, 243, 104–114.
Slabu, L. M., Escera, C., Grimm, S., & Costa-Faidella, J. (2010). Early change detection in humans as revealed by auditory brainstem and middle-latency evoked potentials. European Journal of Neuroscience, 32, 859–865.
Slabu, L., Grimm, S., & Escera, C. (2012). Novelty detection in the human auditory brainstem. The Journal of Neuroscience, 32(4), 1447–1452.
Smith, J. C., Marsh, J. T., & Brown, W. S. (1975). Far-field recorded frequency-following responses: Evidence for the locus of brainstem sources. Electroencephalography and Clinical Neurophysiology, 39(5), 465–472.
Sohmer, H., Pratt, H., & Kinarti, R. (1977). Sources of frequency following responses (FFR) in man. Electroencephalography and Clinical Neurophysiology, 42(5), 656–664.
Strait, D. L., Hornickel, J., & Kraus, N. (2011). Subcortical processing of speech regularities underlies reading and music aptitude in children. Behavioral and Brain Functions, 7, 44. Doi:10.1186/1744-9081-7-44
Suga, N. (2008). Role of corticofugal feedback in hearing. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 194, 169–183.
Suga, N., Xiao, Z., Ma, X., & Li, W. (2002). Plasticity and corticofugal modulation for hearing in adults animals. Neuron, 36, 9–18.
Taaseh, N., Yaron, A., & Nelken, I. (2011). Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS ONE, 6, e23369. Doi:10.1371/journal.pone.0023369
Trujillo-Barreto, N. J., Aubert-Vázquez, E., & Valdés-Sosa, P. A. (2004). Bayesian model averaging in EEG/MEG imaging. NeuroImage, 21, 1300–1319.
Ulanovsky, N., Las, L., Farkas, D., & Nelken, I. (2004). Multiple time scales of adaptation in auditory cortex neurons. The Journal of Neuroscience, 24, 10440–10453.
Ulanovsky, N., Las, L., & Nelken, I. (2003). Processing of low-probability sounds by cortical neurons. Nature Neuroscience, 6, 391–398.
Umbricht, D., Schmid, L., Koller, R., Vollenweider, F. X., et al. (2000). Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: Implications for models of cognitive deficits in schizophrenia. Archives of General Psychiatry, 57, 1139–1147.
Winkler, I. (2007). Interpreting the mismatch negativity. Journal of Psychophysiology, 27, 147–163.
Winkler, I., Denham, S. L., & Nelken, I. (2009). Modeling the auditory scene: Predictive regularity representations and perceptual objects. Trends in Cognitive Sciences, 13, 532–540.
Yvert, B., Crouzeix, A., Bertrand, O., Seither-Preisler, A., & Pantev, C. (2001). Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. Cerebral Cortex, 11, 411–423.
Zarnowiec, K., Costa-Faidella, J., & Escera, C. (2014). Fine-grained violations in rhythmic auditory stimulation modulate the human frequency-following response. International Journal of Psychophysiology, 94, 167.
Acknowledgments
Thanks to all the members of the Brainlab-Cognitive Neuroscience Research Group, past and present, for their work contributing to this research and for being a continuous source of inspiration. Special thanks are for Katarzyna Zarnowiec for her esteemed contribution to set up the FFR experiments and to her and Natàlia Gorina-Careta for their comments on an earlier version of the manuscript. This work was supported by grants from the Fundaçao Bial (Porto, Portugal: 30/12), Fundación Alicia Koplowitz (Madrid, Spain), the Spanish Ministry of Economy and Competitiveness (MINECO: PSI2012-37174, PSI2013-49348-EXPLORA, PSI2015-63664-P), the Catalan Government (SGR2014-177), and the ICREA Acadèmia Distinguished Professorship award.
Compliance with Ethics Requirements
Carles Escera declared that he had no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Escera, C. (2017). The Role of the Auditory Brainstem in Regularity Encoding and Deviance Detection. In: Kraus, N., Anderson, S., White-Schwoch, T., Fay, R., Popper, A. (eds) The Frequency-Following Response. Springer Handbook of Auditory Research, vol 61. Springer, Cham. https://doi.org/10.1007/978-3-319-47944-6_5
Download citation
DOI: https://doi.org/10.1007/978-3-319-47944-6_5
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-47942-2
Online ISBN: 978-3-319-47944-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)