Hyperconnectivity during screen-based stories listening is associated with lower narrative comprehension in preschool children exposed to screens vs dialogic reading: An EEG study

English version

Autoři: Rola Farah ^aff001; Raya Meri ^aff001; Darren S. Kadis ^aff002; John Hutton ^aff004; Thomas DeWitt ^aff004; Tzipi Horowitz-Kraus ^aff001
Působiště autorů: Educational Neuroimaging Center, Faculty of Education in Science and Technology, Technion, Haifa, Israel ^aff001; Division of Neurology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America ^aff002; Pediatric Neuroimaging Research Consortium, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America ^aff003; Department of Pediatrics, College of Medicine, University of Cincinnati, Cincinnati, Ohio, United States of America ^aff004; Reading and Literacy Discovery Center, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225445

Souhrn

Objectives

Dialogic reading (DR) is a shared storybook reading intervention previously shown to have a positive effect on both literacy and general language skills. The aim of this study was to examine the effect of DR compared to screen-based intervention on electrophysiological markers supporting narrative comprehension using EEG.

Methods

Thirty-two typically developing preschoolers, ages 4 to 6 years, were assigned to one of two intervention groups: Dialogic Reading Group (DRG, n = 16) or Screen Story Group (SSG, n = 16). We examined the effect of intervention type using behavioral assessment and a narrative comprehension task with EEG.

Results

The DRG showed improved vocabulary and decreased functional connectivity during the stories-listening task, whereas the SSG group showed no changes in vocabulary or connectivity. Significantly decreased network strength and transitivity and increased network efficiency were observed in the DRG following intervention. Greater network strength and transitivity at follow-up were correlated with increased vocabulary.

Conclusions

The results suggest the beneficial effect of DR in preschool-age children on vocabulary and EEG-bands related to attention in the ventral stream during narrative comprehension. Decreased functional connectivity may serve as a marker for language gains following reading intervention.

Significance

DR intervention for preschool-age children may reduce interfering connections related to attention, which is related to better narrative comprehension.

Klíčová slova:

Children – Electroencephalography – Vision – Attention – Language – Literacy – Neural pathways – Vocabulary

Zdroje

1. High PCK. Literacy promotion: an essential component of primary care pediatric practice. Pediatrics. 2014;134:404–9. doi: 10.1542/peds.2014-1384 24962987

2. Dewalt DA, Berkman ND, Sheridan S, Lohr KN, Pignone MP. Literacy and health outcomes: a systematic review of the literature. Journal of General Internal Medicine,. 2004;19(12):1228–39. doi: 10.1111/j.1525-1497.2004.40153.x 15610334

3. Green CM, Berkule SB, Dreyer BP, Fierman AH, Huberman HS, Klass PE, et al. Maternal literacy and associations between education and the cognitive home environment in low-income families. Archives of Pediatric and Adolescent Medicine. 2009;163(9):832–7.

4. Dehaene S. Reading in the brain: The new science of how we read. New York, NY: Penguin; 2009.

5. Dehaene S, Cohen L. Cultural recycling of cortical maps. Neuron. 2007;56(2):384–98. Epub 2007/10/30. doi: 10.1016/j.neuron.2007.10.004 17964253.

6. Schlaggar BL, McCandliss BD. Development of neural systems for reading. Annual review of neuroscience. 2007;30:475–503. doi: 10.1146/annurev.neuro.28.061604.135645 17600524.

7. Ben Shalom D, Poeppel D. Functional Anatomic Models of Language: Assembling the Pieces. tHE Neuroscientist. 2008;14:119–27. doi: 10.1177/1073858407305726 17911215

8. Sandak R, Mencl WE, Frost J, Pugh KR. The Neurobiological Basis of Skilled and Impaired Reading: Recent Findings and New Directions. SCIENTIFIC STUDIES OF READING. 2004;8(3):273–92.

9. Horowitz-Kraus T, Vannest JJ, Gozdas E, Holland SK. Greater Utilization of Neural-Circuits Related to Executive Functions is Associated with Better Reading: A Longitudinal fMRI Study Using the Verb Generation Task. Frontiers in human neuroscience. 2014;8:447. doi: 10.3389/fnhum.2014.00447 24999322; PubMed Central PMCID: PMC4064667.

10. Giraud A, Poeppel D. Cortical oscillations and speech processing: emerging computational principles and operations. Nature neuroscience. 2012;15(4):511–7. doi: 10.1038/nn.3063 22426255

11. Whitehurst GJ, Lonigan CJ. Child development and emergent literacy. Child development. 1998;69(3):848–72. 9680688.

12. Kuhl P. Early Language Learning and Literacy: Neuroscience Implications for Education. Mind Brain and Education. 2011;5(3):128–42.

13. Horowitz-Kraus T, Hutton JS. From emergent literacy to reading: how learning to read changes a child's brain. Acta paediatrica (Oslo, Norway: 1992). 2015a;104(7):648–56. Epub 2015/04/08. doi: 10.1111/apa.13018 25847632.

14. Sacchi E, Laszlo S. An event-related potential study of the relationship between N170 lateralization and phonological awareness in developing readers. Neuropsychologia. 2016; 91:415–25. doi: 10.1016/j.neuropsychologia.2016.09.001 27614290

15. Turkeltaub PE, Gareau L, Flowers DL, Zeffiro TA, Eden GF. Development of neural mechanisms for reading. Nature neuroscience. 2003;6(7):767–73. Epub 2003/05/20. doi: 10.1038/nn1065 12754516.

16. Hutton JS, Horowitz-Kraus T, Mendelsohn AL, DeWitt T, Holland SK. Home Reading Environment and Brain Activation in Preschool Children Listening to Stories. Pediatrics. 2015;136(3):466–78. Epub 2015/08/12. doi: 10.1542/peds.2015-0359 26260716.

17. O'Farrellya C, Doylea O, Victorya G, Palamaro-Munsellc E. Shared reading in infancy and later development: Evidence from an early intervention. Journal of Applied Developmental Psychology. 2010;54:69–83.

18. Bus AG, Van IJzendoorn MH, Pellegrini AD. Joint Book Reading Makes for Success in Learning to Read: A Meta-Analysis on Intergenerational Transmission of Literacy. Review of Educational Research. 1995;65(1):1–21. doi: 10.3102/00346543065001001

19. Crain-Thoreson C, Dal PS. Do Early Talkers Become Early Readers? Linguistic Precocity, Preschool Language, and Emergent Literacy. Developmental psychology. 1992;28(3):421–9.

20. DeBaryshe BD. Joint picture-book reading correlates of early oral language skill. Journal of Child Language. 1993;20(2): 455–61 doi: 10.1017/s0305000900008370 8376479

21. Sénéchal M, LeFevre JA, Hudson E, Lawson EP. Knowledge of storybooks as a predictor of young children's vocabulary. Journal of Educational Psychology. 1996;88(3):520–36.

22. Derrfuss J, Brass M, Neumann J, Yves von Cramon D. Involvement of the Inferior Frontal Junction in Cognitive Control: Meta-Analyses of Switching and Stroop Studies. Human brain mapping. 2005;25:22–34. doi: 10.1002/hbm.20127 15846824

23. Hutton J, Phelan K, Horowitz-Kraus T, Dudley J, Altaye M, DeWitt T, et al. Shared Reading Quality and Brain Activation during Sto ry Listening in Preschool-Age Children. The Journal of pediatrics. 2017;191:204–12. doi: 10.1016/j.jpeds.2017.08.037 29173308

24. Horowitz-Kraus T, Hutton J, Phelan K, Holland SK. Maternal reading fluency is positively associated with greater functional connectivity between the child's future reading network and regions related to executive functions and language processing in preschool-age children. Brain and cognition. 2018.

25. Justice LM, Pullen PC. Promising interventions for promoting emergent literacy skills: Three evidence-based approaches. Topics in Early Childhood Special Education. 2003;23:99–113.

26. Whitehurst GJ, Arnold DS, Epstein JN, Angell AL, Smith M, Fischel JE. A picture book reading intervention in day care and home for children from low-income families. Developmental Psychology,. 1994;30(5):679–89.

27. Twait E, Farah R, Shamir N, Horowitz-Kraus T. Dialogic Reading Intervention in Preschoolers is Related to Greater Cognitive Control: an EEG Study. Acta Pediatrica. Accepted.

28. Kuhl PK RR, Bosseler A, Lin JF, Imada T. Infants' brain responses to speech suggest analysis by synthesis. Proc Natl Acad Sci U S A 2014;111(31):11238–45. doi: 10.1073/pnas.1410963111 25024207

29. Kuhl PK, Tsao FM, Liu HM. Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(15):9096–101. Epub 2003/07/16. doi: 10.1073/pnas.1532872100 12861072; PubMed Central PMCID: PMC166444.

30. Kuhl PK. Brain Mechanisms in Early Language Acquisition. Neuron. 2010;67(5):713–27. doi: 10.1016/j.neuron.2010.08.038 20826304

31. Kuhl PK. Early language aquisition: cracking the speech code. NATURE REVIEWS, NEUROSCIENCE. 2010;831(5):831–43.

32. Dehaene-Lambertz G, Hertz-Pannier L, Dubois J, Meriaux S, Roche A, Sigman M, et al. Functional organization of perisylvian activation during presentation of sentences in preverbal infants. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(38):14240–5. Epub 2006/09/14. doi: 10.1073/pnas.0606302103 16968771; PubMed Central PMCID: PMC1599941.

33. Telkemeyer S, Rossi S, Koch SP, Nierhaus T, Steinbrink J, Poeppel D, et al. Sensitivity of newborn auditory cortex to the temporal structure of sounds. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009;29(47):14726–33. doi: 10.1523/JNEUROSCI.1246-09.2009 19940167.

34. Holland SK, Vannest J, Mecoli M, Jacola LM, Tillema JM, Karunanayaka PR, et al. Functional MRI of language lateralization during development in children. International journal of audiology. 2007;46(9):533–51. Epub 2007/09/11. doi: 10.1080/14992020701448994 17828669; PubMed Central PMCID: PMC2763431.

35. Sroka MC, Vannest J, Maloney TC, Horowitz-Kraus T, Byars AW, Holland SK. Relationship between receptive vocabulary and the neural substrates for story processing in preschoolers. Brain Imaging Behav. 2015;9(1):43–55. Epub 2014/12/24. doi: 10.1007/s11682-014-9342-8 25533780.

36. Horowitz-Kraus T, Vannest JJ, Holland SK. Overlapping neural circuitry for narrative comprehension and proficient reading in children and adolescents. Neuropsychologia. 2013;51(13):2651–62. Epub 2013/09/14. doi: 10.1016/j.neuropsychologia.2013.09.002 24029377.

37. Vannest JJ, Karunanayaka PR, Altaye M, Schmithorst VJ, Plante EM, Eaton KJ, et al. Comparison of fMRI data from passive listening and active-response story processing tasks in children. Journal of magnetic resonance imaging: JMRI. 2009;29(4):971–6. Epub 2009/03/24. doi: 10.1002/jmri.21694 19306445; PubMed Central PMCID: PMC2763568.

38. Federmeier KD, Wlotko EW, Meyer AM. What's ‘Right’ in Language Comprehension: Event‐Related Potentials Reveal Right Hemisphere Language Capabilities. Lang Linguist Compass. 2008;1(2(1)):1–17.

39. Alday PM, Schlesewsky M, Bornkessel-Schlesewsky I. Electrophysiology Reveals the Neural Dynamics of Naturalistic Auditory Language Processing: Event-Related Potentials Reflect Continuous Model Updates. ENEURO. 2017;0311-16.2017.

40. Luo H, Poeppel D. Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron. 2007;54(6):1001–10. doi: 10.1016/j.neuron.2007.06.004 17582338

41. Plvermoller F, Birbaumer N, Lutzenberger W, Mohr B. High-Frequency Brain Activity: Its Possible Role in Attention, Perception and Language Processing. Progress in Neurobiology. 1997;52:427–45. doi: 10.1016/s0301-0082(97)00023-3 9304700

42. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Research Reviews 1999;29:169–19. doi: 10.1016/s0165-0173(98)00056-3 10209231

43. Anderson AJ, Perone S. Developmental change in the resting state electroencephalogram: insights into cognition and the brain. Brain and cognition. 2018;126:40–52. doi: 10.1016/j.bandc.2018.08.001 30144749

44. Perone S, Palanisamy J, Carlson SM. Developmental change in brain rhythms from early to middle childhood: Links to executive function. Developmental science. 2018;21(6):e12691. doi: 10.1111/desc.12691 29863816

45. Başar E. A review of alpha activity in integrative brain function: fundamental physiology, sensory coding, cognition and pathology. International Journal of Psychophysiology. 2012;86(1)(6):1–24. doi: 10.1016/j.ijpsycho.2012.07.002 22820267

46. Cheung MC, Chan AS, Han YM, Sze SL. Brain activity during resting state in relation to academic performance. Journal of Psychophysiology. 2014;28(47-53).

47. Başar E. A review of alpha activity in integrative brain function: fundamental physiology, sensory coding, cognition and pathology. International Journal of Psychophysiology. 2012;86(1):1–24. doi: 10.1016/j.ijpsycho.2012.07.002 22820267

48. Herrmann CS, Strüber D, Helfrich RF, Engel AK. EEG oscillations: from correlation to causality. International Journal of Psychophysiology. 2016;103:12–21. doi: 10.1016/j.ijpsycho.2015.02.003 25659527

49. Conners CK. Conners’ Kiddie Continuous Performance Test. North Tonawanda. NY: Multi-Health Systems; 2006.

50. Wechsletr D. The Wechsler Preschool and Primary Scale of Intelligence, Third Edition (WPPSI-III). 2002.

51. Shatil E. Shatil test for the assesment of early childhood literacy. Israel: Ach Publishers; 2000.

52. Schmithorst VJ, Holland SK, Plante E. Development of effective connectivity for narrative comprehension in children. Neuroreport. 2007;18(14):1411–5. Epub Epub 2007/08/23. doi: 10.1097/WNR.0b013e3282e9a4ef 00001756-200709170-00001. 17712265

53. Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data. Computational Intelligence and Neuroscience. 2011;1:1–9.

54. Oostenveld R, Stegeman DF, Praamstra P, van Oosterom A. Brain symmetry and topographic analysis of lateralized event-related potentials. Clinical Neurophysiology. 2003;114(7):1194–202 doi: 10.1016/s1388-2457(03)00059-2 12842715

55. Mazziotta JC, Toga AW, Evans AC, Fox PT, Lancaster J, Zilles K, et al. International Consortium for Brain Mapping. Four-dimensional probabilistic atlas of the human brain. Journal of the American Medical Informatics Association (JAMIA). 2001;8(5):401–30.

56. Van Veen BD, van Drongelen W, Yuchtman M, Suzuki A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE transactions on bio-medical engineering 1997;44(9):867–80. doi: 10.1109/10.623056 9282479

57. Barnes‐Davis ME, Merhar SL, Holland SK, Kadis DS. Extremely preterm children exhibit increased interhemispheric connectivity for language: findings from fMRI‐constrained MEG analysis. Developlmental Scoence. 2018. doi: doi.org/10.1111/desc.12669

58. Zalesky AFA, Bullmore ET. Network-based statistic: identifying differences in brain networks. Neuroimage. 2010;53(4):1197–207. doi: 10.1016/j.neuroimage.2010.06.041 20600983

59. Newman MEJ. The structure and function of complex networks. SIAM Rev. 2003;45:167–256.

60. Latora V, Marchiori M. Efficient behaviour of small-world networks. Phys Rev Lett. 2001;87:198701. doi: 10.1103/PhysRevLett.87.198701 11690461

61. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage. 2010;52(3):1059–69. Epub 2009/10/13. doi: 10.1016/j.neuroimage.2009.10.003 19819337.

62. Watts DJ, Strogatz SH. Collective dynamics of 'small-world' networks. Nature. 1998;393(6684):440-2. Epub 1998/06/12. doi: 10.1038/30918 9623998.

63. Kuhl PK. Is speech learning 'gated' by the social brain? Developmental science. 2007;10(1):110–20. Epub 2006/12/22. doi: DESC572 [pii] doi: 10.1111/j.1467-7687.2007.00572.x 17181708.

64. Moon C, Lagercrantz H, Kuhl PK. Language experienced in utero affects vowel perception after birth: a two-country study. ACTA Paediatra. 2013;102(2):156–60.

65. Kuhl PK, Conboy BT, Coffey-Corina S, Padden D, Rivera-Gaxiola M, Nelson T. Phonetic learning as a pathway to language: new data and native language magnet theory expanded (NLM-e). Phil Trans R Soc B 2008;363:979–1000. doi: 10.1098/rstb.2007.2154 17846016

66. Kalashnikova M, Varghese P, Di Liberto GM, Lalor EC, Burnham D. Infant-directed speech facilitates seven-month-old infants’ cortical tracking of speech. Nature. 2018. www.nature.com/scientificreports.

67. Somsen RJM, Van-Klooster BJ, Van-der-Molen MW, Van-Leeuwen HM. Growth spurts in brain maturation during middle childhood as indexed by EEG power spectra. Biol Psychol 1997;44(187–209).

68. Reeves B, Thorson E, Rothschild ML, McDonald D, Hirsch J, Goldstein R. Attention to television: Intrastimulus effects of movement and scene changes on alpha variation over time. International Journal of Neuroscience. 1985;27: 241–55. doi: 10.3109/00207458509149770 4044133

69. Weinstein S, Appel V, Weinstein C. Brain activity responses to magazine and television advertising. Journal of Advertising Research. 1980; 20:57–63.