Article published In: The Mental Lexicon
Vol. 20:1 (2025) ► pp.67–92
Haemodynamic correlate of the mismatch negativity response reflects memory-trace activation for spoken words
An fMRI study
Kristina S. Memetova | Saint Petersburg State UniversitySaint Petersburg | National Research Centre ‘Kurchatov Institute’Moscow
Published online: 18 November 2025
https://doi.org/10.1075/ml.24031.sht
https://doi.org/10.1075/ml.24031.sht
Abstract
Cortical memory circuits that represent words in the brain form the foundation of our mental lexicon; yet, their
architecture remains poorly understood. A valuable approach to probing these representations is measuring the Mismatch Negativity
(MMN), an electrophysiological brain response sensitive to various psycholinguistic variables; however, its specificity to lexical
processing remains debated. To scrutinise its properties as a neural index of word-specific memory trace activity, we adapted the
classical passive auditory oddball design to fMRI and recorded the BOLD (blood oxygenation level-dependent) correlate of the MMN
elicited by words of different lexical frequencies and by phonologically matched control pseudowords. The results showed
significant BOLD-MMN responses in bilateral superior-temporal and middle-temporal cortices. Crucially, these activations were more
expressed for meaningful words than meaningless pseudowords, indicating BOLD-MMN sensitivity to the stimulus’ lexicality. We also
found the left temporal activity to be more pronounced for high- than low-frequency words, the effect not found for their
pseudoword analogues, further confirming the lexical nature of these responses. This pattern of results is best explained by the
automatic activation of long-term memory traces for real words formed in the process of previous linguistic experience whose
intensity determines the strength of connectivity within these circuits and thus the magnitude of their activation, which thereby
reflects the respective stimuli’s status in the brain's mental lexicon.
Keywords: language, word, brain, cortex, temporal lobe, lexical frequency, fMRI, BOLD, mismatch negativity (MMN), memory trace
Article outline
- Introduction
- Methods
- Participants
- Stimuli
- Image acquisition
- Data analysis
- Results
- Discussion
- Conclusions
- Acknowledgements
- Notes
References
References (81)
Alexandrov, A. A., Boricheva, D. O., Pulvermüller, F., & Shtyrov, Y. (2011). Strength
of word-specific neural memory traces assessed electrophysiologically. PLoS
One, 6(8), e22999.
Alho, K. (1995). Cerebral
generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound
changes. Ear and
Hearing, 16(1), 38–51.
Annett, M. (1970). A
classification of hand preference by association analysis. British Journal of
Psychology, 61(3), 303–321.
Argyriou, P., Byfield, S., & Kita, S. (2015). Semantics
is crucial for the right-hemisphere involvement in metaphor processing: Evidence from mouth asymmetry during
speaking. Laterality, 20(2), 191–210.
Baayen, R. H., Shaoul, C., Willits, J., & Ramscar, M. (2016). Comprehension
without segmentation: A proof of concept with naive discriminative learning. Language,
cognition and
neuroscience, 31(1), 106–128.
Brett, M., Anton, J.-L., Valabregue, R., & Poline, J. B. (2002). Region
of interest analysis using an SPM toolbox. Neuroimage, 16(CD-ROM)(Suppl
2), #497.
Chee, M. W. L., Westphal, C., Goh, J., Graham, S., & Song, A. W. (2003). Word
frequency and subsequent memory effects studied using event-related
fMRI. NeuroImage, 20(2), 1042–1051.
Chuang, Y. Y., Vollmer, M. L., Shafaei-Bajestan, E., Gahl, S., Hendrix, P., Baayen, R. H. (2021). The
processing of pseudoword form and meaning in production and comprehension: A computational modeling approach using linear
discriminative learning. Behav Res
Methods. 53(3):945–976.
de Zubicaray, G. I., McMahon, K. L., Eastburn, M. M., Finnigan, S., & Humphreys, M. S. (2005). fMRI
evidence of word frequency and strength effects in recognition memory. Brain Research.
Cognitive Brain
Research, 24(3), 587–598.
Escera, C., Alho, K., Winkler, I., & Näätänen, R. (1998). Neural
mechanisms of involuntary attention to acoustic novelty and change. Journal of Cognitive
Neuroscience, 10(5), 590–604.
Fahimi Hnazaee, M., Khachatryan, E., Chehrazad, S., Kotarcic, A., De Letter, M., & Van Hulle, M. M. (2020). Overlapping
connectivity patterns during semantic processing of abstract and concrete words revealed with multivariate Granger Causality
analysis. Scientific
Reports, 10(1), 2803.
Fitzgerald, K., & Todd, J. (2020). Making
Sense of Mismatch Negativity. Frontiers in
Psychiatry, 111, 468.
Gahl, S., Baayen, R. H. (2024). Time
and thyme again: Connecting English spoken word duration to models of the mental
lexicon. Language, 100(4), 623–670.
Garagnani, M., Shtyrov, Y., & Pulvermüller, F. (2009). Effects
of attention on what is known and what is not: MEG evidence for functionally discrete memory
circuits. Frontiers in human
neuroscience, 31, 10.
Garagnani, M., Wennekers, T., & Pulvermüller, F. (2008). A
neuroanatomically grounded Hebbian-learning model of attention-language interactions in the human
brain. European Journal of
Neuroscience, 27(2), 492–513.
Gaskell, M. G., & Marslen-Wilson, W. D. (1997). Integrating
form and meaning: A distributed model of speech perception. Language and cognitive
Processes, 12(5–6), 613–656.
Giard, M. H., 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(6), 627–640.
Gnedykh, D., Tsvetova, D., Mkrtychian, N., Blagovechtchenski, E., Kostromina, S., & Shtyrov, Y. (2024). tDCS
of right-hemispheric Wernicke’s area homologue affects contextual learning of novel
lexicon. Neurobiology of Learning and
Memory, 1079051,
Gomot, M., Giard, M. H., Roux, S., Barthelemy, C., & Bruneau, N. (2000). Maturation
of frontal and temporal components of mismatch negativity (MMN) in
children. Neuroreport, 11(14), 3109–3112.
Grisoni, L., Moseley, R. L., Motlagh, S., Kandia, D., Sener, N., Pulvermüller, F., Roepke, S., & Mohr, B. (2019). Prediction
and Mismatch Negativity Responses Reflect Impairments in Action Semantic Processing in Adults With Autism Spectrum
Disorders. Frontiers in Human
Neuroscience, 131. [URL].
Grundei, M., Schröder, P., Gijsen, S., & Blankenburg, F. (2023). EEG
mismatch responses in a multimodal roving stimulus paradigm provide evidence for probabilistic inference across audition,
somatosensation, and vision. Human Brain
Mapping, 44(9), 3644–3668.
Hall, C. N., Howarth, C., Kurth-Nelson, Z., & Mishra, A. (2016). Interpreting
BOLD: Towards a dialogue between cognitive and cellular neuroscience. Philosophical
Transactions of the Royal Society B: Biological
Sciences, 371(1705), 20150348.
Hanna, J., Cappelle, B., & Pulvermüller, F. (2017). Spread
the word: MMN brain response reveals whole-form access of discontinuous particle verbs. Brain
and
Language, 1751, 86–98.
Hauk, O., Davis, M. H., Pulvermüller, F., & Pulvermüller, F. (2008). Modulation
of brain activity by multiple lexical and word form variables in visual word recognition: A parametric fMRI
study. Neuroimage, 42(3), 1185–1195.
Hauk, O., Johnsrude, I., & Pulvermüller, F. (2004). Somatotopic
representation of action words in human motor and premotor
cortex. Neuron, 41(2), 301–307.
Heitmeier, M., Chuang, Y. Y., Baayen, R. H. (2023). How
trial-to-trial learning shapes mappings in the mental lexicon: Modelling lexical decision with linear discriminative
learning. Cogn
Psychol. 1461:101598.
Hendrix, P., Ramscar, M., Baayen, R. H. (2019). NDRA:
A single route model of response times in the reading aloud task based on discriminative
learning. PLoS
ONE, 14(7):e0218802.
Hendrix, P., Sun, C. C. (2021). A
word or two about nonwords: Frequency, semantic neighborhood density, and orthography-to-semantics consistency effects for
nonwords in the lexical decision task. Journal of Experimental Psychology: Learning, Memory,
and
Cognition, 47(1):157–183.
Herrmann, B., Maess, B., Hasting, A. S., & Friederici, A. D. (2009). Localization
of the syntactic mismatch negativity in the temporal cortex: An MEG
study. NeuroImage, 48(3), 590–600.
Hultén, A., van Vliet, M., Kivisaari, S., Lammi, L., Lindh-Knuutila, T., Faisal, A., & Salmelin, R. (2021). The
neural representation of abstract words may arise through grounding word meaning in language
itself. Hum Brain
Mapp. 42(15):4973–4984.
Huster, R. J., Debener, S., Eichele, T., & Herrmann, C. S. (2012). Methods
for Simultaneous EEG-fMRI: An Introductory Review. Journal of
Neuroscience, 32(18), 6053–6060.
Huth, A. G., de Heer, W. A., Griffiths, T. L., Theunissen, F. E., & Gallant, J. L. (2016). Natural
speech reveals the semantic maps that tile human cerebral
cortex. Nature, 532(7600), 453–458.
Jacobsen, T., Bäß, P., Roye, A., Winkler, I., Schröger, E., & Horváth, J. (2021). Word
class and word frequency in the MMN looking glass. Brain and
Language, 2181, 104964.
Lai, X.-F., Yan, Z., Shao, L.-C., & Duan, F. (2022). [Asymmetric
response mechanism of auditory event related potentials]. Sheng Li Xue
Bao: [Acta Physiologica
Sinica], 74(4), 563–573.
Leminen, A., Leminen, M., Kujala, T., & Shtyrov, Y. (2013). Neural
dynamics of inflectional and derivational morphology processing in the human
brain. Cortex, 49(10).
Lotto, A. J., Hickok, G. S., Holt, L. L. (2009). Reflections
on mirror neurons and speech perception. Trends Cogn
Sci 13(3):110–114.
Lyashevskaya, O. N., Sharov, S. A. Frequency
dictionary of modern Russian language (based on national corpus of Russian language, Moscow, Azbukovnik, 2009 ([URL])
MacGregor, L. J., & Shtyrov, Y. (2013). Multiple
routes for compound word processing in the brain: Evidence from EEG. Brain and
language, 126(2), 217–229.
Mathiak, K., Rapp, A., Kircher, T. T. J., Grodd, W., Hertrich, I., Weiskopf, N., Lutzenberger, W., & Ackermann, H. (2002). Mismatch
responses to randomized gradient switching noise as reflected by fMRI and whole-head
magnetoencephalography. Human Brain
Mapping, 16(3), 190–195.
Menning, H., Zwitserlood, P., Schoning, S., Hihn, H., Bolte, J., Dobel, C., Mathiak, K., & Lutkenhoner, B. (2005). Pre-attentive
detection of syntactic and semantic
errors. Neuroreport, 16(1), 77–80.
Näätänen, R., Kujala, T., & Light, G. (2019). The
Mismatch Negativity: A Window to the Brain. Oxford University Press.
Näätänen, R., Paavilainen, P., Rinne, T., & Alho, K. (2007). The
mismatch negativity (MMN) in basic research of central auditory processing: A review. Clin
Neurophysiol, 118(12), 2544–2590.
Paavilainen, P., Alho, K., Reinikainen, K., Sams, M., & Näätänen, R. (1991). Right
hemisphere dominance of different mismatch negativities. Electroencephalography and Clinical
Neurophysiology, 78(6), 466–479.
Papeo, L., Lingnau, A., Agosta, S., Pascual-Leone, A., Battelli, L., Caramazza, A. (2015). The
Origin of Word-related Motor Activity. Cerebral
Cortex, 25(6), 1668–1675,
Pettigrew, C. M., Murdoch, B. E., Ponton, C. W., Finnigan, S., Alku, P., Kei, J., Sockalingam, R., & Chenery, H. J. (2004). Automatic
auditory processing of English words as indexed by the mismatch negativity, using a multiple deviant
paradigm. Ear and
Hearing, 25(3), 284–301.
Pettigrew, C. M., Murdoch, B. M., Chenery, H. J., & Kei, J. (2004). The
relationship between the mismatch negativity (MMN) and psycholinguistic models of spoken word
processing. Aphasiology, 18(1), 3–28.
Politzer-Ahles, S., & Im, S. (2020). Mismatch
Negativity Is Not Always Modulated by Lexicality. Frontiers in Human
Neuroscience, 141, 556457.
Pulvermüller, F. (1999). Words
in the brain’s language. Behavioral and Brain
Sciences, 221, 253–336.
(2013). How
neurons make meaning: brain mechanisms for embodied and abstract-symbolic semantics. Trends in
Cognitive
Sciences, 17(9), 458 — 470.
Pulvermüller, F., Kujala, T., Shtyrov, Y., Simola, J., Tiitinen, H., Alku, P., Alho, K., Martinkauppi, S., Ilmoniemi, R. J., & Näätänen, R. (2001). Memory
traces for words as revealed by the mismatch
negativity. Neuroimage, 14(3), 607–616.
Pulvermüller, F., & Shtyrov, Y. (2006). Language
outside the focus of attention: The mismatch negativity as a tool for studying higher cognitive
processes. Prog
Neurobiol, 79(1), 49–71.
Pulvermüller, F., Shtyrov, Y., & Ilmoniemi, R. (2005). Brain
signatures of meaning access in action word recognition. Journal of cognitive
neuroscience, 17(6), 884–892.
Pulvermüller, F., Shtyrov, Y. (2009). Spatiotemporal
signatures of large-scale synfire chains for speech processing as revealed by MEG. Cerebral
Cortex, 19(1), 79–88.
Rissman, J., Eliassen, J. C., & Blumstein, S. E. (2003). An
event-related FMRI investigation of implicit semantic priming. J Cogn
Neurosci, 15(8), 1160–1175.
Robson, M. D., Dorosz, J. L., & Gore, J. C. (1998). Measurements
of the Temporal fMRI Response of the Human Auditory Cortex to Trains of
Tones. NeuroImage, 7(3), 185–198.
Sánchez, A., Carreiras, M., & Paz-Alonso, P. M. (2023). Word
frequency and reading demands modulate brain activation in the inferior frontal
gyrus. Scientific
Reports, 13(1), 17217.
Shtyrov, Y. (2010). Automaticity
and attentional control in spoken language processing: Neurophysiological evidence. Mental
Lexicon, 5(2), 255–276.
(2011). Fast
mapping of novel word forms traced neurophysiologically. Frontiers in
Psychology, 21: 340.
Shtyrov, Y., & Pulvermüller, F. (2007). Early
MEG activation dynamics in the left temporal and inferior-frontal cortex reflect semantic context
integration. Journal of Cognitive
Neuroscience, 19(10) 1633–1642,
Shtyrov, Y., Pulvermüller, F., & Kujala, T. (2010). Interaction
between language and attention systems: early automatic lexical processing? Journal of
Cognitive
Neuroscience, 22(7),1465–78,
Shtyrov, Y., Butorina, A., Nikolaeva, A., & Stroganova, T. (2014). Automatic
ultrarapid activation and inhibition of cortical motor systems in spoken word
comprehension. Proceedings of the National Academy of Sciences of the United States of
America, 111(18), E1918–23.
Shtyrov, Y., Hauk, O., & Pulvermüller, F. (2004). Distributed
neuronal networks for encoding category-specific semantic information: The mismatch negativity to action
words. European Journal of
Neuroscience, 19(4), 1083–1092.
Shtyrov, Y., Kimppa, L., Pulvermüller, F., & Kujala, T. (2011). Event-related
potentials reflecting the frequency of unattended spoken words: A neuronal index of connection strength in lexical memory
circuits? NeuroImage, 55(2).
Shtyrov, Y., Kirsanov, A., & Shcherbakova, O. (2019). Explicitly
slow, implicitly fast, or the other way around? Brain mechanisms for word
acquisition. Frontiers in human
neuroscience, 131, 116.
Shtyrov, Y., Kujala, T., Palva, S., Ilmoniemi, R. J., & Naatanen, R. (2000). Discrimination
of speech and of complex nonspeech sounds of different temporal structure in the left and right cerebral
hemispheres. Neuroimage, 12(6), 657–663.
Shtyrov, Y., Osswald, K., & Pulvermüller, F. (2008). Memory
traces for spoken words in the brain as revealed by the hemodynamic correlate of the mismatch
negativity. Cerebral
Cortex, 18(1), 29–37.
Shtyrov, Y., Pihko, E., & Pulvermüller, F. (2005). Determinants
of dominance: Is language laterality explained by physical or linguistic features of
speech? Neuroimage, 27(1), 37–47.
Shtyrov, Y., & Pulvermüller, F. (2002). Neurophysiological
evidence of memory traces for words in the human
brain. Neuroreport, 13(4), 521–525.
Sittiprapaporn, W., Chindaduangratn, C., Tervaniemi, M., & Khotchabhakdi, N. (2003). Preattentive
processing of lexical tone perception by the human brain as indexed by the mismatch negativity
paradigm. Annals of the New York Academy of
Sciences, 9991, 199–203.
Tsang, Y.-K., Zou, Y., & Tse, C.-Y. (2022). Semantic
Transparency in Chinese Compound Word Processing: Evidence from Mismatch
Negativity. Neuroscience, 4901, 216–223.
Ulanov, M., Kopytin, G., Bermúdez-Margaretto, B., Ntoumanis, I., Gorin, A., Moiseenko, O., Blagovechtchenski, E., Moiseeva, V., Shestakova, A., Jääskeläinen, I., & Shtyrov, Y. (2024). Regionally
specific cortical lateralization of abstract and concrete verb processing: Magnetic mismatch negativity
study. Neuropsychologia, 1951, 108800.
Wennekers, T., Garagnani, M., & Pulvermüller, F. (2006). Language
models based on Hebbian cell assemblies. J Physiol
Paris, 100(1–3), 16–30.
Wilson, S. M., Isenberg, A. L., & Hickok, G. (2009). Neural
correlates of word production stages delineated by parametric modulation of psycholinguistic
variables. Hum Brain
Mapp, 30(11), 3596–3608.
Winkler, I., & Czigler, I. (2012). Evidence
from auditory and visual event-related potential (ERP) studies of deviance detection (MMN and vMMN) linking predictive coding
theories and perceptual object representations. International Journal of
Psychophysiology, 83(2), 132–143.
Woolnough, O., Donos, C., Murphy, E., Rollo, P. S., Roccaforte, Z. J., Dehaene, S., & Tandon, N. (2023). Spatiotemporally
distributed frontotemporal networks for sentence reading. Proceedings of the National Academy
of Sciences of the United States of
America, 120(17), e2300252120.
Zevin, J. D., Datta, H., Maurer, U., Rosania, K. A., & McCandliss, B. D. (2010). Native
language experience influences the topography of the mismatch negativity to speech. Frontiers
in Human Neuroscience, 41, 212.
Zhao, S., Wu, Y., Tsang, Y.-K., Sui, X., & Zhu, Z. (2021). Morpho-semantic
analysis of ambiguous morphemes in Chinese compound word recognition: An fMRI
study. Neuropsychologia, 1571, 107862.
Zhuang, J., Tyler, L. K., Randall, B., Stamatakis, E. A., & Marslen-Wilson, W. D. (2012). Optimally
Efficient Neural Systems for Processing Spoken Language. Cerebral
Cortex.
Zinke, K., Thöne, L., Bolinger, E. M., & Born, J. (2018). Dissociating
Long and Short-term Memory in Three-Month-Old Infants Using the Mismatch Response to Voice
Stimuli. Frontiers in
Psychology, 91. [URL].
