Sleep-based memory processing facilitates grammatical generalization: Evidence from targeted memory reactivation

Brain and Language

Volumn 167, Issue , 2017, Pages 83-93

  Batterink, Laura J ^a   Paller, Ken A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Abstraction; Generalization; Language acquisition; Learning; Memory consolidation; Sleep; Syntax; Targeted memory reactivation

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; FAST SPINDLE DENSITY; FEMALE; GRAMMAR; GRAMMATICAL GENERALIZATION; HUMAN; INFORMATION PROCESSING; LANGUAGE; LEARNING; MALE; MEMORY; NONREM SLEEP; PROCEDURES; REM SLEEP; SLEEP; SLEEP SPINDLE; SLOW SPINDLE DENSITY; SLOW WAVE SLEEP; TARGETED MEMORY REACTIVATION; TASK PERFORMANCE; ASSOCIATION; AUDITORY STIMULATION; LANGUAGE DEVELOPMENT; PHYSIOLOGY;

ACOUSTIC STIMULATION; ADULT; CUES; FEMALE; GENERALIZATION (PSYCHOLOGY); HUMANS; LANGUAGE; LANGUAGE DEVELOPMENT; MALE; MEMORY; SLEEP;

EID: 84945976245     PISSN: 0093934X     EISSN: 10902155     Source Type: Journal    
DOI: 10.1016/j.bandl.2015.09.003     Document Type: Article

References (56)

1. Antony, J.W., Gobel, E.W., OðHare, J.K., Reber, P.J., Paller, K.A., Cued memory reactivation during sleep influences skill learning. Nature Neuroscience 15 (2012), 1114–1116.
2. Arzi, A., Shedlesky, L., Ben-Shaul, M., Nasser, K., Oksenberg, A., Hairston, I.S., Sobel, N., Humans can learn new information during sleep. Nature Neuroscience 15 (2012), 1460–1464.
3. Batterink, L., Oudiette, D., Reber, P.J., Paller, K., Sleep facilitates learning a new linguistic rule. Neuropsychologia 65 (2014), 169–179.
4. Bendor, D., Wilson, M.A., Biasing the content of hippocampal replay during sleep. Nature Neuroscience 15 (2012), 1439–1444.
5. Berko, J., The child's learning of English morphology. Word 14 (1958), 150–177.
6. Chang, G.Y., Knowlton, B.J., Visual feature learning in artificial grammar classification. Journal of Experimental Psychology: Learning, Memory, and Cognition 30 (2004), 714–722.
7. Cousins, J.N., El-Deredy, W., Parkes, L.M., Hennies, N., Lewis, P.A., Cued memory reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence. The Journal of Neuroscience 34 (2014), 15870–15876.
8. Creery, J.D., Oudiette, D., Antony, J.W., Paller, K.A., Targeted memory reactivation during sleep depends on prior learning. Sleep 38 (2015), 755–763.
9. De Gennaro, L., Ferrara, M., Sleep spindles: An overview. Sleep Medicine Reviews 7 (2003), 423–440.
10. Diekelmann, S., Büchel, C., Born, J., Rasch, B., Labile or stable: Opposing consequences for memory when reactivated during waking and sleep. Nature Neuroscience 14 (2011), 381–386.
11. Dienes, Z., Berry, D., Implicit learning: Below the subjective threshold. Psychonomic Bulletin & Review 4 (1997), 3–23.
12. Dienes, Z., Scott, R., Measuring unconscious knowledge: Distinguishing structural knowledge and judgment knowledge. Psychological Research 69 (2005), 338–351.
13. Djonlagic, I., Rosenfeld, A., Shohamy, D., Myers, C., Gluck, M., Stickgold, R., Sleep enhances category learning. Learning and Memory 16 (2009), 751–755.
14. Durrant, S.J., Cairney, S.A., Lewis, P.A., Overnight consolidation aids the transfer of statistical knowledge from the medial temporal lobe to the striatum. Cerebral Cortex 23 (2013), 2467–2478.
15. Durrant, S., Taylor, C., Cairney, S., Lewis, P., Sleep-dependent consolidation of statistical learning. Neuropsychologia 49 (2011), 1322–1331.
16. Ellenbogen, J.M., Hu, P.T., Payne, J.D., Titone, D., Walker, M.P., Human relational memory requires time and sleep. Proceedings of the National Academy of Sciences of the United States of America 104 (2007), 7723–7728.
17. Emmons, W.H., Simon, C.W., The non-recall of material presented during sleep. American Journal of Psychology 69 (1956), 76–81.
18. Fenn, K.M., Nusbaum, H.C., Margoliash, D., Consolidation during sleep of perceptual learning of spoken language. Nature 425 (2003), 614–616.
19. Ferrarelli, F., Huber, R., Peterson, M.J., Massimini, M., Murphy, M., Riedner, B.A.,.. Tononi, G., Reduced sleep spindle activity in schizophrenia. American Journal of Psychiatry 164 (2007), 483–492.
20. Forkstam, C., Hagoort, P., Fernandez, G., Ingvar, M., Petersson, K.M., Neural correlates of artificial syntactic structure classification. NeuroImage 32 (2006), 956–967.
21. Fuentemilla, L., Miro, J., Ripolles, P., Vila-Ballo, A., Juncadella, M., Castaner, S.,.. Rodriguez-Fornells, A., Hippocampus-dependent strengthening of targeted memories via reactivation during sleep in humans. Current Biology 23 (2013), 1769–1775.
22. Gaskell, M.G., Warker, J., Lindsay, S., Forst, R., Guest, J., Snowdon, R., Stackhouse, A., Sleep underpins the plasticity of language production. Psychological Science 25 (2014), 1457–1465.
23. Gómez, R.L., Bootzin, R.R., Nadel, L., Naps promote abstraction in language-learning infants. Psychological Science 17 (2006), 670–674.
24. Grigg-Damberger, M.M., The AASM scoring manual four years later. Journal of Clinical Sleep Medicine 8 (2012), 323–332.
25. Hauser, M.D., Chomsky, N., Fitch, W.T., The faculty of language: What is it, who has it, and how did it evolve?. Science 298 (2002), 1569–1579.
26. Johnson, J.S., Newport, E.L., Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language. Cognitive Psychology 21 (1989), 60–99.
27. Knoblauch, V., Martens, W.L., Wirz-Justice, A., Cajochen, C., Human sleep spindle characteristics after sleep deprivation. Clinical Neurophysiology 114 (2003), 2258–2267.
28. Knowlton, B.J., Squire, L.R., The information acquired during artificial grammar learning. Journal of Experimental Psychology: Learning, Memory, and Cognition 20 (1994), 79–91.
29. Knowlton, B.J., Squire, L.R., Artificial grammar learning depends on implicit acquisition of both abstract and exemplar-specific information. Journal of Experimental Psychology: Learning, Memory, and Cognition 22 (1996), 169–181.
30. Lewis, P.A., Durrant, S.J., Overlapping memory replay during sleep builds cognitive schemata. Trends in Cognitive Sciences 15 (2011), 343–351.
31. Lieberman, M.D., Chang, G.Y., Chiao, J., Bookheimer, S.Y., Knowlton, B.J., An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience 16 (2004), 427–438.
32. Mander, B.A., Santhanam, S., Saletin, J.M., Walker, M.P., Wake deterioration and sleep restoration of human learning. Current Biology 21 (2011), R183–R184.
33. Menn, L., Ratner, N.B., Methods for studying language production. Menn, L., Ratner, N.B., (eds.) In the beginning was the wug: Forty years of language-elicitation studies, 2000, Lawrence Erlbaum Associates, Hillsdale, NJ, 1–23.
34. Meulemans, T., Van der Linden, M., Associative chunk strength in artificial grammar learning. Journal of Experimental Psychology: Learning, Memory, and Cognition 23 (1997), 1007–1028.
35. Milner, C.E., Fogel, S.M., Cote, K.A., Habitual napping moderates motor performance improvements following a short daytime nap. Biological Psychology 73 (2006), 141–156.
36. Nieuwenhuis, I.L.C., Folia, V., Forkstam, C., Jensen, O., Petersson, K.M., Sleep promotes the extraction of grammatical rules. PLoS ONE, 8, 2013, e65046.
37. Nir, Y., Staba, R.J., Andrillon, T., Vyazovskiy, V.V., Cirelli, C., Fried, I., Tononi, G., Regional slow waves and spindles in human sleep. Neuron 70 (2011), 153–169.
38. Nishida, M., Walker, M.P., Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE, 4, 2007, e341.
39. Oudiette, D., Antony, J.W., Creery, J.D., Paller, K.A., The role of memory reactivation during wakefulness and sleep in determining which memories endure. The Journal of Neuroscience 33 (2013), 6672–6678.
40. Oudiette, D., Paller, K.A., Upgrading the sleeping brain with targeted memory reactivation. Trends in Cognitive Sciences 17 (2013), 142–149.
41. Perruchet, P., Pacteau, C., Synthetic grammar learning: Implicit rule abstraction or explicit fragmentary knowledge?. Journal of Experimental Psychology: General 119 (1990), 264–275.
42. Pinker, S., Jackendoff, R., The faculty of language: What's special about it?. Cognition 95 (2005), 201–236.
43. Rasch, B., Buchel, C., Gais, S., Born, J., Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315 (2007), 1426–1429.
44. Rihm, J.S., Diekelmann, S., Born, J., Rasch, B., Reactivating memories during sleep by odors: Odor specificity and associated changes in sleep oscillations. Journal of Cognitive Neuroscience 26 (2014), 1806–1818.
45. Rudoy, J.D., Voss, J.L., Westerbrg, C.E., Paller, K.A., Strengthening individual memories by reactivating them during sleep. Science, 326, 2009, 1079.
46. Saffran, J.R., The use of predictive dependencies in language learning. Journal of Memory and Language 44 (2001), 493–515.
47. Saffran, J.R., Constraints on statistical language learning. Journal of Memory and Language 47 (2002), 172–196.
48. Schabus, M., Dang-Vu, T.T., Albouy, G., Balteau, E., Boly, M., Carrier, J.,.. Maquet, P., Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proceedings of the National Academy of Sciences 104 (2007), 13164–13169.
49. Schonauer, M., Geisler, T., Gais, S., Strengthening procedural memories by reactivation in sleep. Journal of Cognitive Neuroscience 26 (2013), 143–153.
50. Schreiner, T., Rasch, B., Boosting vocabulary learning by verbal cueing during sleep. Cerebral Cortex, 2014 pii: bhu139. [Epub ahead of print].
51. Shadmehr, R., Moussavi, Z.M.K., Spatial generalization from learning dynamics of reaching movements. The Journal of Neuroscience 20 (2000), 7807–7815.
52. Simon, C.W., Emmons, W.H., EEG, consciousness and sleep. Science 124 (1956), 1066–1069.
53. Stickgold, R., Walker, M.P., Sleep-dependent memory triage: Evolving generalization through selective processing. Nature Neuroscience 16 (2013), 139–145.
54. Urakami, Y., Relationships between sleep spindles and activities of cerebral cortex as determined by simultaneous EEG and MEG recording. Journal of Clinical Neurophysiology 25 (2008), 13–24.
55. Wagner, U., Gais, S., Haider, H., Verleger, R., Born, J., Sleep inspires insight. Nature 427 (2004), 352–355.
56. Weber-Fox, C.M., Neville, H.J., Maturational constraints on functional specializations for language processing: ERP and behavioral evidence in bilingual speakers. Journal of Cognitive Neuroscience 8 (1996), 231–256.