[en] Hebb repetition learning is a fundamental learning mechanism for sequential knowledge,
such as language. However, still little is known about its development. This
fMRI study examined the developmental neural substrates of Hebb repetition learning
and its relation with reading abilities in a group of 49 children aged from 6 to
12 years. In the scanner, the children carried out an immediate serial recall task for
syllable sequences of which some sequences were repeated several times over the
course of the session (Hebb repetition sequences). The rate of Hebb repetition learning
was associated with modulation of activity in the medial temporal lobe.
Importantly, for the age range studied here, learning-related medial temporal lobe
modulation was independent of the age of the children. Furthermore, we observed
an association between regular and irregular word reading abilities and the neural
substrates of Hebb repetition learning. This study suggests that the functional neural
substrates of Hebb repetition learning do not undergo further maturational changes
in school age children, possibly because they are sustained by implicit sequential
learning mechanisms which are considered to be fully developed by that age. Importantly,
the neural substrates of Hebb learning remain significant determinants of children's
learning abilities, such as reading.
Research center :
PsyNCog - Psychologie et Neuroscience Cognitives - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Attout, Lucie ; Université de Liège - ULiège > Département de Psychologie > Département de Psychologie
Ordonez Magro, Laura
Szmalec, Arnaud
Majerus, Steve ; Université de Liège - ULiège > Département de Psychologie > Département de Psychologie
Language :
English
Title :
The developmental neural substrates of Hebb repetition learning and their link with reading ability
Publication date :
27 February 2020
Journal title :
Human Brain Mapping
ISSN :
1065-9471
eISSN :
1097-0193
Publisher :
John Wiley & Sons, Hoboken, United States - New York
Volume :
41
Pages :
3956-3969
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Amso, D., & Davidow, J. (2012). The development of implicit learning from infancy to adulthood: Item frequencies, relations, and cognitive flexibility. Developmental Psychobiology, 54(6), 664–673. https://doi.org/10.1002/dev.20587
Andersson, J. L., Hutton, C., Ashburner, J., Turner, R., & Friston, K. (2001). Modeling geometric deformations in EPI time series. NeuroImage, 13(5), 903–919. https://doi.org/10.1006/nimg.2001.0746
Archibald, L. M. D., & Joanisse, M. F. (2013). Domain-specific and domain-general constraints on word and sequence learning. Memory and Cognition, 41(2), 268–280. https://doi.org/10.3758/s13421-012-0259-4
Attout, L., Ordonez Magro, L., Szmalec, A., & Majerus, S. (2019). The developmental neural substrates of item and serial order components of verbal working memory. Human Brain Mapping, 40(5), 1541–1553. https://doi.org/10.1002/hbm.24466
Bauer, P. J. (2008). Toward a neuro-developmental account of the development of declarative memory. Developmental Psychobiology, 50(1), 19–31. https://doi.org/10.1002/dev.20265
Bogaerts, L., Szmalec, A., De Maeyer, M., Page, M. P. A., & Duyck, W. (2016). The involvement of long-term serial-order memory in reading development: A longitudinal study. Journal of Experimental Child Psychology, 145, 139–156. https://doi.org/10.1016/j.jecp.2015.12.008
Bogaerts, L., Szmalec, A., Hachmann, W. M., Page, M. P. A., & Duyck, W. (2015). Linking memory and language: Evidence for a serial-order learning impairment in dyslexia. Research in Developmental Disabilities, 43–44, 106–122. https://doi.org/10.1016/j.ridd.2015.06.012
Crone, E. A., Wendelken, C., Donohue, S., van Leijenhorst, L., & Bunge, S. A. (2006). Neurocognitive development of the ability to manipulate information in working memory. Proceedings of the National Academy of Sciences of the United States of America, 103(24), 9315–9320. https://doi.org/10.1073/pnas.0510088103
Davachi, L., & DuBrow, S. (2015). How the hippocampus preserves order: The role of prediction and context. Trends in Cognitive Sciences, 19(2), 92–99. https://doi.org/10.1016/j.tics.2014.12.004
De Visscher, A., Szmalec, A., Van Der Linden, L., & Noël, M.-P. (2015). Serial-order learning impairment and hypersensitivity-to-interference in dyscalculia. Cognition, 144, 38–48. https://doi.org/10.1016/j.cognition.2015.07.007
DeMaster, D. M., & Ghetti, S. (2013). Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex, 49(6), 1482–1493. https://doi.org/10.1016/j.cortex.2012.08.004
DeMaster, D. M., Pathman, T., Lee, J. K., & Ghetti, S. (2014). Structural development of the hippocampus and episodic memory: Developmental differences along the anterior/posterior axis. Cerebral Cortex, 24(11), 3036–3045. https://doi.org/10.1093/cercor/bht160
Dienes, Z. (2011). Bayesian versus orthodox statistics: Which side are you on? Perspectives on Psychological Science, 6(3), 274–290. https://doi.org/10.1177/1745691611406920
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America, 113(28), 7900–7905. https://doi.org/10.1073/pnas.1602413113
Ellis, C. T., & Turk-Browne, N. B. (2018). Infant fMRI: A model system for cognitive neuroscience. Trends in Cognitive Sciences, 22(5), 375–387. https://doi.org/10.1016/j.tics.2018.01.005
Evans, J. L., Saffran, J. R., & Robe-Torres, K. (2009). Statistical learning in children with specific language impairment. Journal of Speech, Language, and Hearing Research, 52(2), 321–335. https://doi.org/10.1044/1092-4388(2009/07-0189
Finn, A. S., Kalra, P. B., Goetz, C., Leonard, J. A., Sheridan, M. A., & Gabrieli, J. D. E. (2016). Developmental dissociation between the maturation of procedural memory and declarative memory. Journal of Experimental Child Psychology, 142, 212–220. https://doi.org/10.1016/j.jecp.2015.09.027
Gagnon, S., Foster, J. K., Turcotte, J., & Jongenelis, S. (2004). Involvement of the hippocampus in implicit learning of supra-span sequences: The case of SJ. Cognitive Neuropsychology, 21(8), 867–882. https://doi.org/10.1080/02643290342000609
Gathercole, S. E., Frankish, C. R., Pickering, S. J., & Peaker, S. (1999). Phonotactic influences on short-term memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 25(1), 84–95.
Gebauer, D., Fink, A., Kargl, R., Reishofer, G., Koschutnig, K., Purgstaller, C., … Enzinger, C. (2012). Differences in brain function and changes with intervention in children with poor spelling and reading abilities. PLoS One, 7(5), e38201. https://doi.org/10.1371/journal.pone.0038201
Ghetti, S., DeMaster, D. M., Yonelinas, A. P., & Bunge, S. A. (2010). Developmental differences in medial temporal lobe function during memory encoding. Journal of Neuroscience, 30(28), 9548–9556. https://doi.org/10.1523/JNEUROSCI.3500-09.2010
Giedd, J. N., Rumsey, J. M., Castellanos, F. X., Rajapakse, J. C., Kaysen, D., Vaituzis, A. C., … Rapoport, J. L. (1996). A quantitative MRI study of the corpus callosum in children and adolescents. Developmental Brain Research, 91(2), 274–280. https://doi.org/10.1016/0165-3806(95)00193-X
Gogtay, N., Nugent, T. F., Herman, D. H., Ordonez, A., Greenstein, D., Hayashi, K. M., … Thompson, P. M. (2006). Dynamic mapping of normal human hippocampal development. Hippocampus, 16(8), 664–672. https://doi.org/10.1002/hipo.20193
Gould, J. H., & Glencross, D. J. (1990). Do children with a specific reading disability have a general serial-ordering deficit? Neuropsychologia, 28(3), 271–278. https://doi.org/10.1016/0028-3932
Guérard, K., Saint-Aubin, J., Boucher, P., & Tremblay, S. (2011). The role of awareness in anticipation and recall performance in the hebb repetition paradigm: Implications for sequence learning. Memory and Cognition, 39(6), 1012–1022. https://doi.org/10.3758/s13421-011-0084-1
Hebb, D. O. (1961). Distinctive features of learning in the higher animal. In J. F. Delafresnaye (Ed.), Brain mechanisms and learning (pp. 37–46). Oxford, England: Blackwell.
Hsieh, L. T., Gruber, M. J., Jenkins, L. J., & Ranganath, C. (2014). Hippocampal activity patterns carry information about objects in temporal context. Neuron, 81(5), 1165–1178. https://doi.org/10.1016/j.neuron.2014.01.015
Hulme, C., Maughan, S., & Brown, G. D. A. (1991). Memory for familiar and unfamiliar words: Evidence for a long-term memory contribution to short-term memory span. Journal of Memory and Language, 30(6), 685–701. https://doi.org/10.1016/0749-596X(91)90032-F
Hulme, C., Roodenrys, S., Brown, G. D. A., & Mercer, R. (1995). The role of long-term memory mechanisms in memory span. British Journal of Psychology, 86(4), 527–536. https://doi.org/10.1111/j.2044-8295.1995.tb02570.x
Hutton, C., Bork, A., Josephs, O., Deichmann, R., Ashburner, J., & Turner, R. (2002). Image distortion correction in fMRI: A quantitative evaluation. NeuroImage, 16(1), 217–240. https://doi.org/10.1006/nimg.2001.1054
Insausti, R., Cebada-Sánchez, S., & Marcos, P. (2010). Postnatal development of the human hippocampal formation. Advances in Anatomy, Embryology and Cell Biology, 206, 1–86.
Jeffreys, H. (1961). Theory of probability. Oxford, England: Clarendon.
Kalm, K., Davis, M. H., & Norris, D. (2013). Individual sequence representations in the medial temporal lobe. Journal of Cognitive Neuroscience, 25(7), 1111–1121. https://doi.org/10.1162/jocn_a_00378
Kharitonova, M., Winter, W., & Sheridan, M. A. (2015). As working memory grows: A developmental account of neural bases of working memory capacity in 5- to 8-year old children and adults. Journal of Cognitive Neuroscience, 27(9), 1775–1778. https://doi.org/10.1162/jocn_a_00824
Klingberg, T., Forssberg, H., & Westerberg, H. (2002). Increased brain activity in frontal and parietal cortex underlies the development of visuospatial working memory capacity during childhood. Journal of Cognitive Neuroscience, 14(1), 1–10. https://doi.org/10.1162/089892902317205276
Lehmann, M., & Hasselhorn, M. (2007). Variable memory strategy use in children's adaptive intratask learning behavior: Developmental changes and working memory influences in free recall. Child Development, 78(4), 1068–1082. https://doi.org/10.1111/j.1467-8624.2007.01053.x
Levenshtein, V. I. (1966). Binary codes capable of correcting deletions, insertions, and reversals. Soviet Physics Doklady, 10(8), 707–710.
Majerus, S., Bastin, C., Poncelet, M., Van der Linden, M., Salmon, E., Collette, F., … Maquet, P. (2007). Short-term memory and the left intraparietal sulcus: Focus of attention? Further evidence from a face short-term memory paradigm. NeuroImage, 35(1), 353–367. https://doi.org/10.1016/j.neuroimage.2006.12.008
Majerus, S., D'Argembeau, A., Martinez Perez, T., Belayachi, S., Van der Linden, M., Collette, F., … Maquet, P. (2010). The commonality of neural networks for verbal and visual short-term memory. Journal of Cognitive Neuroscience, 22(11), 2570–2593. https://doi.org/10.1162/jocn.2009.21378
Majerus, S., & Oberauer, K. (2019). Working memory and serial order: evidence against numerical order codes but for Item-position associations. Journal of Experimental Psychology: Learning Memory and Cognition. https://doi.org/10.1037/xlm0000792.
Majerus, S., Van der Linden, M., Poncelet, M., & Metz-Lutz, M.-N. (2004). Can phonological and semantic short-term memory be dissociated? Further evidence from landau-kleffner syndrome. Cognitive Neuropsychology, 21(5), 491–512. https://doi.org/10.1080/02643290342000104
Maril, A., Davis, P. E., Koo, J. J., Reggev, N., Zuckerman, M., Ehrenfeld, L., … Rivkin, M. J. (2010). Developmental fMRI study of episodic verbal memory encoding in children. Neurology, 75(23), 2110–2116. https://doi.org/10.1212/WNL.0b013e318201526e
Martinez Perez, T., Majerus, S., Mahot, A., & Poncelet, M. (2012). Evidence for a specific impairment of serial order short-term memory in dyslexic children. Dyslexia, 18(2), 94–109. https://doi.org/10.1002/dys.1438
Martinez Perez, T., Majerus, S., Poncelet, M., Martinez, T., Majerus, S., Poncelet, M., … Poncelet, M. (2012). The contribution of short-term memory for serial order to early reading acquisition: Evidence from a longitudinal study. Journal of Experimental Child Psychology, 111(4), 708–723. https://doi.org/10.1016/j.jecp.2011.11.007
Mayes, A., Montaldi, D., & Migo, E. (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11(3), 126–135. https://doi.org/10.1016/j.tics.2006.12.003
Mazaika, P. K., Hoeft, F., Glover, G. H., & Reiss, A. L. (2009). Methods and software for fMRI analysis of clinical subjects. NeuroImage, 47, S58. https://doi.org/10.1016/s1053-8119(09)70238-1
McKelvie, S. J. (1987). Learning and awareness in the Hebb digits task. The Journal of General Psychology, 114(1), 75–88. https://doi.org/10.1080/00221309.1987.9711057
Meulemans, T., Van Der Linden, M., & Perruchet, P. (1998). Implicit sequence learning in children. Journal of Experimental Child Psychology, 69(3), 199–221. https://doi.org/10.1006/jecp.1998.2442
Morey, R. D., & Rouder, J. N. (2011). Bayes factor approaches for testing interval null hypotheses. Psychological Methods, 16(4), 406–419. https://doi.org/10.1037/a0024377
Mosse, E. K., & Jarrold, C. (2008). Hebb learning, verbal short-term memory, and the acquisition of phonological forms in children. Quarterly Journal of Experimental Psychology, 61(4), 505–514. https://doi.org/10.1080/17470210701680779
Naus, M. J., Ornstein, P. A., & Aivano, S. (1977). Developmental changes in memory: The effects of processing time and rehearsal instructions. Journal of Experimental Child Psychology, 23(2), 237–251. https://doi.org/10.1016/0022-0965(77)90102-3
Ofen, N., Chai, X. J., Schuil, K. D. I., Whitfield-Gabrieli, S., & Gabrieli, J. D. E. (2012). The development of brain systems associated with successful memory retrieval of scenes. Journal of Neuroscience, 32(29), 10012–10020. https://doi.org/10.1523/JNEUROSCI.1082-11.2012
Ofen, N., Kao, Y.-C., Sokol-Hessner, P., Kim, H., Whitfield-Gabrieli, S., & Gabrieli, J. D. E. (2007). Development of the declarative memory system in the human brain. Nature Neuroscience, 10, 1198–1205. https://doi.org/10.1038/nn1950
Ordonez Magro, L., Attout, L., Majerus, S., & Szmalec, A. (2018). Short-and long-term memory determinants of novel word form learning. Cognitive Development, 47, 146–157. https://doi.org/10.1016/j.cogdev.2018.06.002
Østby, Y., Tamnes, C. K., Fjell, A. M., Westlye, L. T., Due-Tønnessen, P., & Walhovd, K. B. (2009). Heterogeneity in subcortical brain development: A structural magnetic resonance imaging study of brain maturation from 8 to 30 years. Journal of Neuroscience, 29(38), 11772–11782. https://doi.org/10.1523/JNEUROSCI.1242-09.2009
Page, M. P. A., Cumming, N., Norris, D., Hitch, G. J., & McNeil, A. M. (2006). Repetition learning in the immediate serial recall of visual and auditory materials. Journal of Experimental Psychology: Learning Memory and Cognition, 32(4), 716–733. https://doi.org/10.1037/0278-7393.32.4.716
Paz-Alonso, P. M., Ghetti, S., Donohue, S. E., Goodman, G. S., & Bunge, S. A. (2008). Neurodevelopmental correlates of true and false recognition. Cerebral Cortex, 18(9), 2208–2216. https://doi.org/10.1093/cercor/bhm246
Poncelet, M. (1999). Exploration du rôle des composants phonologique et visuel de la mémoire à court terme dans l'apprentissage des procédures de lecture. (Unpublished doctoral dissertation). University of Liege, Liege, Belgium.
Poncelet, M., & Van der Linden, M. (2003). L'évaluation du stock phonologique de la mémoire de travail: Élaboration d'une épreuve de répétition de non-mots pour population francophone. Revue de Neuropsychologie, 13(3), 375–405.
Raven, C. J., & Raven, J. J. (1998). Progressive matrices couleur. Oxford, England: Oxford Psychologists Press.
Reber, A. S., Walkenfeld, F. F., & Hernstadt, R. (1991). Implicit and explicit learning: Individual differences and IQ. Journal of Experimental Psychology: Learning, Memory, and Cognition, 17(5), 888–896. https://doi.org/10.1037/0278-7393.17.5.888
Roodenrys, S., Hulme, C., & Brown, G. (1993). The development of short-term memory span: Separable effects of speech rate and long-term memory. Journal of Experimental Child Psychology, 56(3), 431–442. https://doi.org/10.1006/jecp.1993.1043
Schapiro, A. C., Turk-Browne, N. B., Botvinick, M. M., & Norman, K. A. (2017). Complementary learning systems within the hippocampus: A neural network modelling approach to reconciling episodic memory with statistical learning. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1711), 20160049. https://doi.org/10.1098/rstb.2016.0049
Siffredi, V., Barrouillet, P., Spencer-Smith, M., Vaessen, M., Anderson, V., & Vuilleumier, P. (2017). Examining distinct working memory processes in children and adolescents using fMRI: Results and validation of a modified Brown-Peterson paradigm. PLoS One, 12(7), 1–22. https://doi.org/10.1371/journal.pone.0179959
Skeide, M. A., Evans, T. M., Mei, E. Z., Abrams, D. A., & Menon, V. (2018). Neural signatures of co-occurring reading and mathematical difficulties. Developmental Science, 21(6), e12680. https://doi.org/10.1111/desc.12680
Smalle, E. H. M., Bogaerts, L., Simonis, M., Duyck, W., Page, M. P. A., Edwards, M. G., & Szmalec, A. (2016). Can chunk size differences explain developmental changes in lexical learning? Frontiers in Psychology, 6. https://doi.org/10.3389/fpsyg.2015.01925
Smalle, E. H. M., Page, M. P. A., Duyck, W., Edwards, M., & Szmalec, A. (2018). Children retain implicitly learned phonological sequences better than adults: A longitudinal study. Developmental Science, 21(5), e12634. https://doi.org/10.1111/desc.12634
Smalle, E. H. M., Panouilleres, M., Szmalec, A., & Möttönen, R. (2017). Language learning in the adult brain: Disrupting the dorsolateral prefrontal cortex facilitates word-form learning. Scientific Reports, 7(1), 1–9. https://doi.org/10.1038/s41598-017-14547-x
Spencer-Smith, M., Ritter, B. C., Mürner-Lavanchy, I., El-Koussy, M., Steinlin, M., & Everts, R. (2013). Age, sex, and performance influence the visuospatial working memory network in childhood. Developmental Neuropsychology, 38(4), 236–255. https://doi.org/10.1080/87565641.2013.784321
Staels, E., & Van den Broeck, W. (2015). No solid empirical evidence for the SOLID (serial order learning impairment) hypothesis of dyslexia. Journal of Experimental Psychology: Learning Memory and Cognition, 41(3), 650–669. https://doi.org/10.1037/xlm0000054
Szmalec, A., Duyck, W., Vandierendonck, A., Mata, A. B., & Page, M. P. A. (2009). The Hebb repetition effect as a laboratory analogue of novel word learning. Quarterly Journal of Experimental Psychology, 62(3), 435–443. https://doi.org/10.1080/17470210802386375
Szmalec, A., Loncke, M., Page, M. P. A., & Duyck, W. (2011). Order or disorder? Impaired Hebb learning in dyslexia. Journal of Experimental Psychology: Learning Memory and Cognition, 37(5), 1270–1279. https://doi.org/10.1037/a0023820
Szmalec, A., Page, M. P. A., & Duyck, W. (2012). The development of long-term lexical representations through Hebb repetition learning. Journal of Memory and Language, 67(3), 342–354. https://doi.org/10.1016/j.jml.2012.07.001
Thomas, K. M., Hunt, R. H., Vizueta, N., Sommer, T., Durston, S., Yang, Y., & Worden, M. S. (2004). Evidence of developmental differences in implicit sequence learning: An fMRI study of children and adults. Journal of Cognitive Neuroscience, 16(8), 1339–1351. https://doi.org/10.1162/0898929042304688
Thomason, M. E., Race, E., Burrows, B., Whitfield-Gabrieli, S., Glover, G. H., & Gabrieli, J. D. E. (2009). Development of spatial and verbal working memory capacity in the human brain. Journal of Cognitive Neuroscience, 21(2), 316–332. https://doi.org/10.1162/jocn.2008.21028
Urbain, C., De Tiège, X., Op De Beeck, M., Bourguignon, M., Wens, V., Verheulpen, D., … Peigneux, P. (2016). Sleep in children triggers rapid reorganization of memory-related brain processes. NeuroImage, 134, 213–222. https://doi.org/10.1016/j.neuroimage.2016.03.055
van den Bosch, G. E., El Marroun, H., Schmidt, M. N., Tibboel, D., Manoach, D. S., Calhoun, V. D., & White, T. J. H. (2014). Brain connectivity during verbal working memory in children and adolescents. Human Brain Mapping, 35(2), 698–711. https://doi.org/10.1002/hbm.22193
Van Essen, D. C., Drury, H. A., Dickson, J., Harwell, J., Hanlon, D., & Anderson, C. H. (2001). An integrated software suite for surface-based analyses of cerebral cortex. Journal of the American Medical Informatics Association, 8, 443–459. https://doi.org/10.1136/jamia.2001.0080443
Wagenmakers, E.-J. (2007). A practical solution to the pervasive problems ofp values. Psychonomic Bulletin & Review, 14(5), 779–804. https://doi.org/10.3758/BF03194105
Wilke, M., Altaye, M., & Holland, S. K. (2017). CerebroMatic: A versatile toolbox for spline-based MRI template creation. Frontiers in Computational Neuroscience, 11(5). https://doi.org/10.3389/fncom.2017.00005.
Yurgelun-Todd, D. A., Killgore, W. D. S., & Cintron, C. B. (2003). Cognitive correlates of medial temporal lobe development across adolescence: A magnetic resonance imaging study. Perceptual and Motor Skills, 96(1), 3–17. https://doi.org/10.2466/pms.2003.96.1.3