Abstract
We offer a model of how human cortex detects changes in the auditory environment. Auditory change detection has recently been the object of intense investigation via the mismatch negativity (MMN). MMN is a preattentive response to sudden changes in stimulation, measured noninvasively in the electroencephalogram (EEG) and the magnetoencephalogram (MEG). It is elicited in the oddball paradigm, where infrequent deviant tones intersperse a series of repetitive standard tones. However, little apart from the participation of tonotopically organized auditory cortex is known about the neural mechanisms underlying change detection and the MMN. In the present study, we investigate how poststimulus inhibition might account for MMN and compare the effects of adaptation with those of lateral inhibition in a model describing tonotopically organized cortex. To test the predictions of our model, we performed MEG and EEG measurements on human subjects and used both small- (<1/3 octave) and large- (>5 octaves) frequency differences between the standard and deviant tones. The experimental results bear out the prediction that MMN is due to both adaptation and lateral inhibition. Finally, we suggest that MMN might serve as a probe of what stimulus features are mapped by human auditory cortex.
Similar content being viewed by others
References
Aitkin LM (1990) The Auditory Cortex: Structural and Functional Bases of Auditory Perception. Chapman and Hall, London.
Aitkin LM, Merzenich MM, Irvine DRF, Clarey JC, Nelson JE (1986) Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus). J. Comp. Neurol. 252:175–185.
Alho K (1995) Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes. Ear & Hearing 16:38–51.
Alho K, Huotilainen M, Tiitinen H, Ilmoniemi RJ, Knuutila J, Nääatänen R (1993) Memory-related processing of complex sound patterns in human auditory cortex: An MEG study. NeuroReport 4:391–394.
Arezzo JC, Vaughan Jr HG, Kraut MA, Steinschneider M, Legatt AD (1986) Intracranial generators of event-related potentials in the monkey. Evoked Potentials. Liss. pp. 174–189.
Bertrand O, Perrin F, Echallier J, Pernier J (1988) Topography and model analysis of auditory evoked potentials: Tonotopic aspects. In: G Pfurtscheller, FH Lopes da Silva, eds. Functional Brain Imaging. Hans Huber, Toronto. pp. 75–82.
Bowery NG, Hudson AL, Price GW (1987) GABAA and GABAB receptor site distribution in the rat central nervous system. Neurosci. 20(2):365–383.
Brugge JF (1982) Auditory cortical areas in primates. In: CN Woolsey, ed. Cortical Sensory Organization. Vol. 3. Multiple Auditory Areas. Humana, Clifton, NJ. pp. 59–70.
Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48:1302–1320.
Connors BW, Malenka RC, Silva LR (1988) Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J. Physiol. (London) 406:443–468.
Cowan N, Winkler I, Teder W, Nääatänen R (1993) Memory prerequisites of mismatch negativity in the auditory event-related potential (ERP). J. Experi. Psychol.: Learning, Memory & Cognition 19(4):909–921.
Csépe V, Karmos G, Molnár M (1987) Evoked potential correlates of stimulus deviance during wakefulness and sleep in cat-animal model of mismatch negativity. Electroencephalography & Clin. Neurophysiol. 66:571–578.
Csépe V, Pantev C, Hoke M, Hampson S, Ross B (1992) Evoked magnetic responses of the human auditory cortex to minor pitch changes: Localization of the mismatch field. Electroencephalography & Clin. Neurophysiol. 84:538–548.
Depireux DA, Simon JZ, Shamma SA (1997) Response-field dynamics in the auditory pathway. Sixth Annual Computational Neuroscience Meeting, Big Sky, Montana.
Douglas RJ, Koch C, Mahowald M, Martin KAC, Suarez HH (1995) Recurrent excitation in neocortical circuits. Nature 269:981–985.
Douglas RJ, Martin KAC (1990) Neocortex. In: GM Sheperd, ed. The Synaptic Organization of the Brain. Oxford University Press, Oxford. pp. 389–438.
Douglas RJ, Martin KAC (1991) A functional microcircuit for cat visual cortex. J. Physiol. 440:735–769.
Eggermont JJ (1991) Rate and synchronization measures of periodicity coding in cat primary auditory cortex. Hearing Res. 56:153–167.
Elberling C, Bak C, Kofoed B, Lebech J, Saermark K(1982) Auditory magnetic fields: Source location and "tonotopic organization" in the right hemisphere of the human brain. Scand. Audiol. 11:61–65.
Ford JM, Hillyard SA (1981) Event related potentials, ERPs, to interruptions of steady rhythm. Psychophysiol. 18:322–330.
Giard MH, Lavikainen J, Reinikainen K, Perrin F, Bertrand O, Pernier J, Nääatänen R (1995) Separate representation of stimulus frequency, intensity, and duration in auditory sensory memory: An event-related potential and dipole-model analysis. J. Cognitive Neurosci. 7(2):133–143.
Giard MH, Perrin F, Pernier J, Bouchet P (1990) Brain generators implicated in processing of auditory stimulus deviance: A topographic event-related potential study. Psychophysiol. 27:627–640.
Halgren E, Baudena P, Clarke JM, Heit G, Liegeois C, Chauvel P, Musolino A (1995) Intracerebral potentials to rare target and distractor auditory and visual stimuli: I. Superior temporal plane and parietal lobe. Electroencephalography & Clin. Neurophysiol. 94:191–220.
Hämäläinen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV (1993) Magnetoencephalography: Theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev. of Modern Physics 65:413–497.
Hari R, Hämäläinen M, Ilmoniemi RJ, Kaukoranta E, Reinikainen K, Salminen J, Alho K, Nääatänen R, Sams M (1984) Responses of the primary auditory cortex to pitch changes in a sequence of tone pips: Neuromagnetic recordings in man. Neurosci. Letters 50:127–132.
Hari R, Joutsiniemi SL, Sarvas J (1988) Spatial resolution of neuromagnetic records: theoretical calculations in a spherical model. Electroencephalography & Clin. Neurophysiol. 71:64–72.
He J, Hashikawa T, Ojima H, Kinouchi Y (1997) Temporal integration and duration tuning in the dorsal zone of cat auditory cortex. J. Neurosci. 17:2615–2625.
Hose B, Langner G, Scheich H (1987) Topographic representation of periodicities in the forebrain of the mynah bird: One map for pitch and rhythm? Brain Res. 422:367–373.
Howard III MA, Volkov IO, Abbas PJ, Damasio H, Ollendick MC, Granner MA (1996) A chronic microelectrode investigation of the tonotopic organization of human auditory cortex. Brain Res. 724:260–264.
Imada T, Fukuda K, Kawakatsu M, Mashiko T, Okada K, Hayashi M, Aihara K, Kotani M (1995) Mismatch fields evoked by a rhythm passage. In: C Baumgartner, L Deecke, G Stroink, SJ Williamson, eds. Biomagnetism: Fundamental Research and Clinical Applications. Elsevier, Amsterdam. pp. 249–252.
Javitt DC, Schroeder CE, Steinschneider M, Arezzo JC, Ritter W, Vaughan Jr HG(1995) Cognitive event-related potentials in human and non-human primates: Implications for the PCP/NMDAmodel of schizophrenia. In: G Karmos, M Molnar, V Csépe, I Czigler, JE Demedt, eds. Perspectives of Event-Related Potentials Research (EEG Supplement 44). Elsevier Science, Amsterdam. pp. 161–175.
Javitt DC, Steinschneider M, Schroeder CE, Vaughan Jr HG, Arezzo JC (1994) Detection of stimulus deviance within primate primary auditory cortex: Intracortical mechanisms of mismatch negativity (MMN) generation. Brain Res. 667:192–200.
Karmos G, Winkler I, Molnár M, Csépe V (1993) Animal model of middle latency auditory evoked responses: Intracortical generators of mismatch negativity. In: HJ Heinze, TF Munte, GR Mangun, eds. New Developments in Event-Related Potentials. Birkhauser, Boston, MA. pp. 95–102.
Knuutila JET, Ahonen AI, Hämäläinen MS, Kajola MJ, Laine PP, Lounasmaa OV, Parkkonen LT, Simola JT, Tesche CD (1993) A 122-channel whole-cortex SQUID system for measuring brain' magnetic field. IEEE Trans. on Magnetism 29:3315–3320.
Koch C, Rapp M, Segev I (1996) A brief history of time (constants). Cerebral Cortex 6:93–101.
Kowalski N, Depireux DA, Shamma SA (1996) Analysis of dynamic spectra in ferret primary auditory cortex. I. Characteristics of single-unit responses to moving ripple spectra. J. Neurophysiol. 76:3503–3523.
Kraus N, McGee T, Littman T, Nicol T, King C (1994) Nonprimary auditory thalamic representation of acoustic change. J. Neurophysiol. 72:1270–1277.
Kropotov JD, Nääatänen R, Sevostianov AV, Alho K, Reinikainen K, Kropotova OV (1995) Mismatch negativity to auditory stimulus change recorded directly from the human temporal cortex. Psychophysiol. 32:418–422.
Lauter JL, Herschovitch P, Formby C, Raichle ME (1985) Tonotopic organization in the human auditory cortex revealed by positron emission tomography. Hearing Res. 20:199–205.
Lu Z-L, Williamson SJ, Kaufman L (1992) Human auditory primary and association cortex have differing lifetimes for activation traces. Brain Res. 572:236–241.
McCormick D (1990) Membrane properties and neurotransmitter actions. In: G Sheperd, ed. The Synaptic Organization of the Brain, 3rd ed. Oxford University Press, Oxford. pp. 32–66.
Merzenich MM, Brugge JF (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res. 50:275–296.
Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65:37–100.
Nääatänen R (1984) In search of a short-duration memory trace of a stimulus in the human brain. In: L Pulkkinen, P Lyytinen, eds. Human Action and Personality: Essays in Honour of Martti Takala. University of Jyväskylä, Jyväskylä, Finland. pp. 29–43.
Nääatänen R (1986) The orienting response theory: An integration of informational and energetical aspects of brain function. In: RGJ Hockey, AWK Gaillard, M Coles, eds. Adaptation to Stress and Task Demands: Energetical Aspects of Human Information Processing. Martinus Nijhoff, Dordrecht. pp. 91–111.
Nääatänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behavioral & Brain Sci. 13:201–288.
Nääatänen R (1992) Attention and Brain Function. Erlbaum, Hillsdale, NJ.
Nääatänen R (1995) The mismatch negativity: A powerful tool for cognitive neuroscience. Ear & Hearing 16:6–18.
Nääatänen R, Alho K (1995) Mismatch negativity: A unique measure of sensory processing in audition. Intl. J. Neurosci. 80:317–337.
Nääatänen R, Gaillard AWK, Mäntysalo S (1978) Early selectiveattention effect on evoked potential reinterpreted. Acta Psychologica 42:313–329.
Nääatänen R, Lehtokoski A, Lennes M, Cheour M, Huotilainen M, Iivonen A, Vainio M, Alku P, Ilmoniemi RJ Luuk A, Allik J, Sinkkonen J, Alho K (1997) Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature 385:432–434.
Nälälatänen R, Paavilainen P, Alho K, Reinikainen K, Sams M (1989a) Do event-related potentials reveal the mechanism of the auditory sensory memory in the human brain? Neurosci. Letters 98:217–221.
Nääatänen R, Paavilainen P, Reinikainen K (1989b) Do event-related potentials to infrequent decrements in duration of auditory stimuli demonstrate a memory trace in man? Neurosci. Letters 107:347–352.
Nääatänen R, Picton TW (1987) The N1 wave of the human electric and magnetic response to sound: A review and an analysis of the component structure. Psychophysiol. 24:375–425.
Nääatänen R, Schröger E, Tervaniemi M, Karakas S, Paavilainen P (1993) Development of a memory trace for complex sound patterns in the human brain. NeuroReport 4:503–506.
Nordby H, Roth WT, Pfefferbaum A (1988) Event-related potentials to time-deviant and pitch-deviant tones. Psychophysiol. 25:249–261.
Paavilainen P, Saarinen J, Tervaniemi M, Nääatänen R (1995) Mismatch negativity to changes in abstract sound features during selective listening. J. Psychophysiol. 9:243–249.
Pandya DN (1995) Anatomy of the auditory cortex. Rev. in Neurol. (Paris) 151(8–9):486–494.
Pantev C, Hoke M, Lehnertz K, Lütkenhoner B, Anogianakis G, Wittkowski W (1988) Tonotopic organization of the human auditory cortex revealed by transient auditory evoked magnetic fields. Electroencephalography & Clin. Neurophysiol. 69:160–170.
Pavlov IP (1927) Conditioned Reflexes. Clarendon Press, Oxford.
Picton TW, Woods DL, Proulx GB (1978) Human auditory sustained potentials. I. The nature of the response. Electroencephalography & Clin. Neurophysiol. 45:186–197.
Rhode WS, Greenberg S (1994) Lateral suppression and inhibition in the cochlear nucleus of the cat. J. Neurophysiol. 71:493–514.
Roberts TPL, Poeppel D (1996) Latency of auditory evoked M100 as a function of tone frequency. NeuroReport 7:1138–1140.
Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in structure of the neocortex. Brain 103:221–244.
Romani GL, Williamson SJ, Kaufman L (1982) Tonotopic organization of the human auditory cortex. Science 216:1339–1340.
Sams M, Hämäläinen M, Antervo A, Kaukoranta E, Reinikainen K, Hari R (1985) Cerebral neuromagnetic responses evoked by short auditory stimuli. Electroencephalography & Clin. Neurophysiol. 61:254–266.
Sams M, Kaukoranta E, Hämäläinen M, Nääatänen R (1991) Cortical activity elicited by changes in auditory stimuli: Different sources for magnetic N100m and mismatch responses. Psychophysiol. 28:21–29.
Schreiner CE (1992) Functional organization of the auditory cortex: Maps and mechanisms. Current Opinion in Neurobiol. 2:516–521.
Schreiner CE, Urbas JV (1988) Representation of amplitude modulation in the auditory cortex of cat. II. Comparison between cortical fields. Hearing Res. 32:49–64.
Schröger E (1994) An event-related potential study of sensory representations of unfamiliar tonal patterns. Psychophysiol. 31:175–181.
Schröger E, Nääatänen R, Paavilainen P (1992) Event-related potentials reveal how non-attended complex sound patterns are represented by the human brain. Neurosci. Letters 146:183–186.
Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J. Neurophysiol. 59:450–467.
Sokolov EN (1960) Neuronal model and orienting reflex. In: MAB Brazier, ed. The Central Nervous System and behavior. Madison Printing, Madison, NJ. pp. 187–276.
Suarez H, Koch C, Douglas R (1995) Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit. J. Neurosci. 15:6700–6719.
Taylor JG, Alavi FN (1993) Mathematical analysis of a competitive network for attention. In: JG Taylor, ed. Mathematical Approaches to Neural Networks. Elsevier, Amsterdam. pp. 341–382.
Tiitinen H, Alho K, Huotilainen M, Ilmoniemi RJ, Simola J, Nääatänen R (1993) Tonotopic auditory cortex and the magnetoencephalographic (MEG) equivalent of the mismatch negativity. Psychophysiol. 30:537–540.
Tiitinen H, May P, Reinikainen K, Nääatänen R (1994) Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372:90–92.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
May, P., Tiitinen, H., Ilmoniemi, R.J. et al. Frequency Change Detection in Human Auditory Cortex. J Comput Neurosci 6, 99–120 (1999). https://doi.org/10.1023/A:1008896417606
Issue Date:
DOI: https://doi.org/10.1023/A:1008896417606