Brain Topography

, Volume 30, Issue 1, pp 136–148 | Cite as

Distinguishing Neural Adaptation and Predictive Coding Hypotheses in Auditory Change Detection

  • Renée M. Symonds
  • Wei Wei Lee
  • Adam Kohn
  • Odelia Schwartz
  • Sarah Witkowski
  • Elyse S. SussmanEmail author
Original Paper


The auditory mismatch negativity (MMN) component of event-related potentials (ERPs) has served as a neural index of auditory change detection. MMN is elicited by presentation of infrequent (deviant) sounds randomly interspersed among frequent (standard) sounds. Deviants elicit a larger negative deflection in the ERP waveform compared to the standard. There is considerable debate as to whether the neural mechanism of this change detection response is due to release from neural adaptation (neural adaptation hypothesis) or from a prediction error signal (predictive coding hypothesis). Previous studies have not been able to distinguish between these explanations because paradigms typically confound the two. The current study disambiguated effects of stimulus-specific adaptation from expectation violation using a unique stimulus design that compared expectation violation responses that did and did not involve stimulus change. The expectation violation response without the stimulus change differed in timing, scalp distribution, and attentional modulation from the more typical MMN response. There is insufficient evidence from the current study to suggest that the negative deflection elicited by the expectation violation alone includes the MMN. Thus, we offer a novel hypothesis that the expectation violation response reflects a fundamentally different neural substrate than that attributed to the canonical MMN.


Attention Event-related brain potentials (ERPs) Expectation Mismatch negativity (MMN) Novelty detection Predictive coding 



This work was supported by the National Institutes of Health (R01 DC004263 to ESS); the Army Research Office (58760LS to ESS, AK, OS), and the Summer Undergraduate Research Program (SURP) of the Albert Einstein College of Medicine (to SW).


  1. Alain C, Cortese F, Picton TW (1999) Event-related brain activity associated with auditory pattern processing. NeuroReport 10:2429–2434CrossRefPubMedGoogle Scholar
  2. Alho K, Huotilainen M, Tiitinen H et al (1993) Memory-related processing of complex sound patterns in human auditory cortex: a MEG study. NeuroReport 4:391–394CrossRefPubMedGoogle Scholar
  3. Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29:7359–7363. doi: 10.1523/JNEUROSCI.0793-09.2009 CrossRefPubMedGoogle Scholar
  4. Bendixen A, Schröger E, Winkler I (2009) I heard that coming: event-related potential evidence for stimulus-driven prediction in the auditory system. J Neurosci 29:8447–8451. doi: 10.1523/JNEUROSCI.1493-09.2009 CrossRefPubMedGoogle Scholar
  5. Blake DT, Merzenich MM (2002) Changes of AI receptive fields with sound density. J Neurophysiol 88:3409–3420. doi: 10.1152/jn.00233.2002 CrossRefPubMedGoogle Scholar
  6. Budd TW, Barry RJ, Gordon E et al (1998) Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. Int J Psychophysiol 31:51–68CrossRefPubMedGoogle Scholar
  7. Butler RA (1968) Effect of changes in stimulus frequency and intensity on habituation of the human vertex potential. J Acoust Soc Am 44:945–950CrossRefPubMedGoogle Scholar
  8. Fishman YI (2013) The mechanisms and meaning of the mismatch negativity. Brain Topogr 27:500–526. doi: 10.1007/s10548-013-0337-3 CrossRefPubMedGoogle Scholar
  9. Fishman YI, Arezzo JC, Steinschneider M (2004) Auditory stream segregation in monkey auditory cortex: effects of frequency separation, presentation rate, and tone duration. J Acoust Soc Am 116:1656–1670CrossRefPubMedGoogle Scholar
  10. Friston K (2005) A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 360:815–836. doi: 10.1098/rstb.2005.1622 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Garrido MI, Friston KJ, Kiebel SJ et al (2008) The functional anatomy of the MMN: a DCM study of the roving paradigm. Neuroimage 42:936–944. doi: 10.1016/j.neuroimage.2008.05.018 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Garrido MI, Kilner JM, Kiebel SJ, Friston KJ (2009a) Dynamic causal modeling of the response to frequency deviants. J Neurophysiol 101:2620–2631. doi: 10.1152/jn.90291.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Garrido MI, Kilner JM, Stephan KE, Friston KJ (2009b) The mismatch negativity: a review of underlying mechanisms. Clin Neurophysiol 120:453–463. doi: 10.1016/j.clinph.2008.11.029 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Giard MH, Perrin F, Pernier J, Bouchet P (1990) Brain generators implicated in the processing of auditory stimulus deviance: a topographic event-related potential study. Psychophysiology 27:627–640CrossRefPubMedGoogle Scholar
  15. Grimm S, Escera C (2012) Auditory deviance detection revisited: evidence for a hierarchical novelty system. Int J Psychophysiol 85:88–92. doi: 10.1016/j.ijpsycho.2011.05.012 CrossRefPubMedGoogle Scholar
  16. Haenschel C, Vernon DJ, Dwivedi P et al (2005) Event-related brain potential correlates of human auditory sensory memory-trace formation. J Neurosci 25:10494–10501. doi: 10.1523/JNEUROSCI.1227-05.2005 CrossRefPubMedGoogle Scholar
  17. Herholz SC, Lappe C, Pantev C (2009) Looking for a pattern: an MEG study on the abstract mismatch negativity in musicians and nonmusicians. BMC Neurosci 10:42. doi: 10.1186/1471-2202-10-42 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jacobsen T, Schroger E, Horenkamp T, Winkler I (2003) Mismatch negativity to pitch change: varied stimulus proportions in controlling effects of neural refractoriness on human auditory event-related brain potentials. Neurosci Lett 344:79–82CrossRefPubMedGoogle Scholar
  19. Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl-d-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci 93:11962–11967. doi: 10.1073/pnas.93.21.11962 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kvale MN, Schreiner CE (2004) Short-term adaptation of auditory receptive fields to dynamic stimuli. J Neurophysiol 91:604–612. doi: 10.1152/jn.00484.2003 CrossRefPubMedGoogle Scholar
  21. Malone BJ, Scott BH, Semple MN (2002) Context-dependent adaptive coding of interaural phase disparity in the auditory cortex of awake macaques. J Neurosci 22:4625–4638PubMedGoogle Scholar
  22. May PJC, Tiitinen H (2010) Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. Psychophysiology 47:66–122. doi: 10.1111/j.1469-8986.2009.00856.x CrossRefPubMedGoogle Scholar
  23. Mill R, Coath M, Wennekers T, Denham SL (2011) A neurocomputational model of stimulus-specific adaptation to oddball and Markov sequences. PLoS Comput Biol 7:e1002117. doi: 10.1371/journal.pcbi.1002117 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Näätänen R, Gaillard AW, Mäntysalo S (1978) Early selective-attention effect on evoked potential reinterpreted. Acta Psychol 42:313–329CrossRefGoogle Scholar
  25. Näätänen R, Paavilainen P, Tiitinen H et al (1993) Attention and mismatch negativity. Psychophysiology 30:436–450CrossRefPubMedGoogle Scholar
  26. Pérez-González D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22:2879–2885. doi: 10.1111/j.1460-9568.2005.04472.x CrossRefPubMedGoogle Scholar
  27. Rao RP, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2:79–87. doi: 10.1038/4580 CrossRefPubMedGoogle Scholar
  28. Squires NK, Squires KC, Hillyard SA (1975) Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr Clin Neurophysiol 38:387–401CrossRefPubMedGoogle Scholar
  29. Sussman E (2007) A new view on the MMN and attention debate: The role of context in processing auditory events. J Psychophysiol 21:164–175. doi: 10.1027/ CrossRefGoogle Scholar
  30. Sussman E, Ritter W, Vaughan HG (1998) Predictability of stimulus deviance and the mismatch negativity. NeuroReport 9:4167–4170. doi: 10.1097/00001756-199812210-00031 CrossRefPubMedGoogle Scholar
  31. Sussman E, Winkler I, Huotilainen M et al (2002) Top-down effects can modify the initially stimulus-driven auditory organization. Cogn Brain Res 13:393–405. doi: 10.1016/S0926-6410(01)00131-8 CrossRefGoogle Scholar
  32. Tiitinen H, May P, Reinikainen K, Naatanen R (1994) Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372:90–92. doi: 10.1038/372090a0 CrossRefPubMedGoogle Scholar
  33. Todorovic A, de Lange FP (2012) Repetition suppression and expectation suppression are dissociable in time in early auditory evoked fields. J Neurosci 32:13389–13395. doi: 10.1523/JNEUROSCI.2227-12.2012 CrossRefPubMedGoogle Scholar
  34. Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6:391–398. doi: 10.1038/nn1032 CrossRefPubMedGoogle Scholar
  35. Wacongne C, Labyt E, van Wassenhove V et al (2011) Evidence for a hierarchy of predictions and prediction errors in human cortex. Proc Natl Acad Sci USA 108:20754–20759. doi: 10.1073/pnas.1117807108 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Renée M. Symonds
    • 1
  • Wei Wei Lee
    • 1
  • Adam Kohn
    • 1
  • Odelia Schwartz
    • 1
  • Sarah Witkowski
    • 1
  • Elyse S. Sussman
    • 1
    Email author
  1. 1.Department of NeuroscienceAlbert Einstein College of MedicineBronxUSA

Personalised recommendations