Cerebellar BOLD signal during the acquisition of a new lexicon predicts its early consolidation

Brain and Language

Volumn 161, Issue , 2016, Pages 33-44

  Lesage, Elise ^a,b   Nailer, Emma L ^a   Miall, R Chris ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Cerebellum; fMRI; Language; Learning; Lexicon; Non motor; Vocabulary; Word association

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN MAPPING; BRAIN REGION; CAUDATE NUCLEUS; CEREBELLUM; CEREBELLUM VERMIS; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; INSULA; LANGUAGE; LEARNING; LEFT HEMISPHERE; LINGUISTICS; MALE; NORMAL HUMAN; PARIETAL CORTEX; PREDICTION; SEMANTICS; SUPERIOR PARIETAL CORTEX; FRONTAL LOBE; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PHYSIOLOGY; RANDOMIZATION; YOUNG ADULT;

BRAIN MAPPING; CEREBELLUM; FEMALE; FRONTAL LOBE; HUMANS; LANGUAGE; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; PARIETAL LOBE; RANDOM ALLOCATION; SEMANTICS; VOCABULARY; YOUNG ADULT;

EID: 84939621165     PISSN: 0093934X     EISSN: 10902155     Source Type: Journal    
DOI: 10.1016/j.bandl.2015.07.005     Document Type: Article

References (97)

1. Abdullaev, Y.G., Bechtereva, N.P., Melnichuk, K.V., Neuronal activity of human caudate nucleus and prefrontal cortex in cognitive tasks. Behavioural Brain Research 97:1–2 (1998), 159–177.
2. Akkal, D., Dum, R.P., Strick, P.L., Supplementary motor area and presupplementary motor area: Targets of basal ganglia and cerebellar output. The Journal of Neuroscience 27:40 (2007), 10659–10673.
3. Albert, N.B., Robertson, E.M., Miall, R.C., The resting human brain and motor learning. Current Biology 19:12 (2009), 1023–1027.
4. Argyropoulos, G.P., Cerebellar theta-burst stimulation selectively enhances lexical associative priming. Cerebellum 10:3 (2011), 540–550.
5. Balsters, J.H., Ramnani, N., Cerebellar plasticity and the automation of first-order rules. The Journal of Neuroscience 31:6 (2011), 2305–2312.
6. Balsters, J.H., Whelan, C.D., Robertson, I.H., Ramnani, N., Cerebellum and cognition: Evidence for the encoding of higher order rules. Cerebral Cortex 23:6 (2013), 1433–1443.
7. Battaglia, F.P., Benchenane, K., Sirota, A., Pennartz, C.M.A., Wiener, S.I., The hippocampus: Hub of brain network communication for memory. Trends in Cognitive Sciences 15:7 (2011), 310–318.
8. Bernard, J.A., Seidler, R.D., Hassevoort, K.M., Benson, B.L., Welsh, R.C., Wiggins, J.L., et al. Resting state cortico-cerebellar functional connectivity networks: A comparison of anatomical and self-organizing map approaches. Frontiers in Neuroanatomy, 6, 2012, 31.
9. Binder, J.R., Desai, R.H., Graves, W.W., Conant, L.L., Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex 19:12 (2009), 2767–2796.
10. Bloedel, J.R., Functional heterogeneity with structural homogeneity – How does the cerebellum operate?. Behavioral and Brain Sciences 15:4 (1992), 666–678.
11. Breitenstein, C., Jansen, A., Deppe, M., Foerster, A.-F., Sommer, J., Wolbers, T., et al. Hippocampus activity differentiates good from poor learners of a novel lexicon. NeuroImage 25:3 (2005), 958–968.
12. Buckner, R.L., Kelley, W.M., Petersen, S.E., Frontal cortex contributes to human memory formation. Nature Neuroscience 2:4 (1999), 311–314.
13. Buckner, R.L., Krienen, F.M., Castellanos, A., Diaz, J.C., Yeo, B.T.T., The organization of the human cerebellum estimated by intrinsic functional connectivity. Journal of Neurophysiology 106:5 (2011), 2322–2345.
14. Cook, M., Murdoch, B., Cahill, L., Whelan, B., Higher-level language deficits resulting from left primary cerebellar lesions. Aphasiology 18:9 (2004), 771–784.
15. Davis, M.H., Maria, A., Betta, D., Macdonald, M.J.E., Gaskell, M.G., Learning and consolidation of novel spoken words. Journal of Cognitive Neuroscience 21:4 (2009), 803–820.
16. De Smet, H.J., Paquier, P., Verhoeven, J., Mariën, P., The cerebellum: Its role in language and related cognitive and affective functions. Brain and Language, 2013, 1–9.
17. Desmond, J.E., Fiez, J.A., Neuroimaging studies of the cerebellum: Language, learning and memory. Trends in Cognitive Sciences 2:9 (1998), 355–362.
18. Devlin, J.T., Russell, R.P., Davis, M.H., Price, C.J., Wilson, J., Moss, H.E., et al. Susceptibility-induced loss of signal: Comparing PET and fMRI on a semantic task. NeuroImage 11:6 Pt 1 (2000), 589–600.
19. Diedrichsen, J., A spatially unbiased atlas template of the human cerebellum. NeuroImage 33:1 (2006), 127–138.
20. Diedrichsen, J., Balsters, J.H., Flavell, J., Cussans, E., Ramnani, N., A probabilistic MR Atlas of the human cerebellum. NeuroImage 46:1 (2009), 39–46.
21. Ding, H., Qin, W., Jiang, T., Zhang, Y., Yu, C., Volumetric variation in subregions of the cerebellum correlates with working memory performance. Neuroscience Letters 508:1 (2012), 47–51.
22. Dobel, C., Junghöfer, M., Breitenstein, C., Klauke, B., Knecht, S., Pantev, C., et al. New names for known things: On the association of novel word forms with existing semantic information. Journal of Cognitive Neuroscience 22:6 (2010), 1251–1261.
23. Dolan, R.J., Fletcher, P.C., Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature 388:6642 (1997), 582–585.
24. Dollaghan, C., Child meets word: “fast mapping” in preschool children. Journal of Speech and Hearing Research 28:3 (1985), 449–454.
25. Dudai, Y., The neurobiology of consolidations, or, how stable is the engram?. Annual Review of Psychology 55 (2004), 51–86.
26. E, K.-H., Chen, S.-H.A., Ho, M.-H.R., Desmond, J.E., A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Human Brain Mapping, 2012 000.
27. Fabbro, F., Moretti, R., Bava, A., Language impairments in patients with cerebellar lesions. Journal of Neurolinguistics 13:2–3 (2000), 173–188.
28. Fedorenko, E., Hsieh, P.-J., Nieto-Castañón, A., Whitfield-Gabrieli, S., Kanwisher, N., New method for fMRI investigations of language: Defining ROIs functionally in individual subjects. Journal of Neurophysiology 104:2 (2010), 1177–1194.
29. Fiez, J.A., Petersen, S.E., Neuroimaging studies of word reading. Proceedings of the National Academy of Sciences 95:3 (1998), 914–921.
30. Fiez, J.A., Petersen, S.E., Cheney, M.K., Raichle, M.E., Impaired non-motor learning and error detection associated with cerebellar damage. Brain 115 (1992), 155–178.
31. Fiez, J.A., Raife, E.A., Petersen, S.E., Balota, D.A., Raichle, E., A positron emission tomography study of the short-term maintenance of verbal information. The Journal of Neuroscience 76:2 (1996), 808–822.
32. Friston, K.J., Zarahn, E., Josephs, O., Henson, R.N., Dale, A.M., Stochastic designs in event-related fMRI. NeuroImage 10:5 (1999), 607–619.
33. Gabrieli, J.D., Cohen, N.J., Corkin, S., The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain and Cognition 7:2 (1988), 157–177.
34. Gebhart, A.L., Petersen, S.E., Thach, W.T., Role of the posterolateral cerebellum in language. Annals of the New York Academy of Sciences 978 (2002), 318–333.
35. Glover, G.H., Li, T.Q., Ress, D., Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magnetic Resonance Imaging 44:1 (2000), 162–167.
36. Gooding, P.A., Mayes, A.R., van Eijk, R., A meta-analysis of indirect memory tests for novel material in organic amnesics. Neuropsychologia 38:5 (2000), 666–676.
37. Habas, C., Kamdar, N., Nguyen, D.A., Prater, K., Beckmann, C.F., Menon, V., et al. Distinct cerebellar contributions to intrinsic connectivity networks. The Journal of Neuroscience 29:26 (2009), 8586–8594.
38. Hanakawa, T., Honda, M., Sawamoto, N., Okada, T., Yonekura, Y., Fukuyama, H., Shibasaki, H., The role of rostral Brodmann area 6 in mental-operation tasks: an integrative neuroimaging approach. Cerebral Cortex 12:11 (2002), 1157–1170.
39. Hayter, A.L., Langdon, D.W., Ramnani, N., Cerebellar contributions to working memory. NeuroImage 36:3 (2007), 943–954.
40. Ito, M., Control of mental activities by internal models in the cerebellum. Nature Reviews Neuroscience 9:4 (2008), 304–313.
41. Jenkins, I.H., Brooks, D.J., Frackowiak, R.S.J., Passingham, F.E., Motor sequence tomography learning: A study with positron emission tomography. Journal of Neuroscience 14:6 (1994), 1775–3790.
42. Kapur, S., Craik, F.I., Tulving, E., Wilson, A.A., Houle, S., Brown, G.M., Neuroanatomical correlates of encoding in episodic memory: Levels of processing effect. Proceedings of the National Academy of Sciences 91:6 (1994), 2008–2011.
43. Kapur, S., Tulving, E., Cabeza, R., McIntosh, A.R., Houle, S., Craik, F.I., The neural correlates of intentional learning of verbal materials: A PET study in humans. Brain Research 4:4 (1996), 243–249.
44. Kawato, M., Kuroda, T., Imamizu, H., Nakano, E., Miyauchi, S., Yoshioka, T., Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Progress in Brain Research 142 (2003), 171–188.
45. Kelly, R.M., Strick, P.L., Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. The Journal of Neuroscience 23:23 (2003), 8432–8444.
46. Klein, A., Andersson, J.L.R., Ardekani, B.A., Ashburner, J., Avants, B., Chiang, M.-C., et al. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 46:3 (2009), 786–802.
47. Kotz, S.A., Schwartze, M., Cortical speech processing unplugged: A timely subcortico-cortical framework. Trends in Cognitive Sciences 14:9 (2010), 392–399.
48. Kriegeskorte, N., Simmons, W.K., Bellgowan, P.S.F., Baker, C.I., Circular analysis in systems neuroscience – The dangers of double dipping. Nature Neuroscience 12:5 (2010), 535–540.
49. Lesage, E., Apps, M.A.J., Hayter, A.L., Beckmann, C.F., Barnes, D., Langdon, D.W., et al. Cerebellar information processing in relapsing-remitting multiple sclerosis (RRMS). Behavioural Neurology 23:1–2 (2010), 39–49.
50. Lesage, E., Morgan, B.E., Olson, A.C., Meyer, A.S., Miall, R.C., Cerebellar rTMS disrupts predictive language processing. Current Biology 22:18 (2012), R794–R795.
51. Linck, J.A., Osthus, P., Koeth, J.T., Bunting, M.F., Working memory and second language comprehension and production: A meta-analysis. Psychonomic Bulletin & Review 21:4 (2014), 861–883.
52. Mariën, P., Ackermann, H., Adamaszek, M., Barwood, C.H.S., Beaton, A., Desmond, J., et al. Consensus paper: Language and the cerebellum: An ongoing enigma. Cerebellum, 2013.
53. Mariën, P., Engelborghs, S., Fabbro, F., De Deyn, P.P., The lateralized linguistic cerebellum: A review and a new hypothesis. Brain and Language 79:3 (2001), 580–600.
54. Marvel, C.L., Desmond, J.E., Functional topography of the cerebellum in verbal working memory. Neuropsychology Review 20:3 (2010), 271–279.
55. McLaughlin, J., Osterhout, L., Kim, A., Neural correlates of second-language word learning: Minimal instruction produces rapid change. Nature Neuroscience 7:7 (2004), 703–704.
56. Miall, R. C. (1998). The cerebellum, predictive control and motor coordination. In Novartis Foundation Symposium, 218, 272–84; discussion 284–90.
57. Miall, R.C., Connecting mirror neurons and forward models. NeuroReport 14:17 (2003), 2135–2137.
58. Miall, R.C., Weir, D.J., Wolpert, D.M., Stein, J.F., Is the cerebellum a smith predictor?. Journal of Motor Behavior 25:3 (1993), 203–216.
59. Middleton, F.A., Strick, P.L., Cerebellar projections to the prefrontal cortex of the primate. The Journal of Neuroscience 21:2 (2001), 700–712.
60. Murdoch, B.E., Whelan, B.-M., Language disorders subsequent to left cerebellar lesions: A case for bilateral cerebellar involvement in language?. Folia Phoniatrica et Logopaedica 59:4 (2007), 184–189.
61. O'Reilly, J.X., Beckmann, C.F., Tomassini, V., Ramnani, N., Johansen-Berg, H., Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cerebral Cortex 20:4 (2010), 953–965.
62. Opitz, B., Friederici, A.D., Interactions of the hippocampal system and the prefrontal cortex in learning language-like rules. NeuroImage 19 (2003), 1730–1737.
63. Osterhout, L., Poliakov, A., Inoue, K., Valentine, G., McLaughlin, J., Pitkanen, I., et al. Second-language learning and changes in the brain. Journal of Neurolinguistics 21:6 (2008), 509–521.
64. Patterson, K., Nestor, P.J., Rogers, T.T., Where do you know what you know? The representation of semantic knowledge in the human brain. Nature Reviews Neuroscience 8:12 (2007), 976–987.
65. Paulesu, E., Frith, C.D., Frackowiak, R.S.J., The neural correlates of the verbal component of working memory. Nature 362 (1993), 342–345.
66. Petersson, K.M., Folia, V., Hagoort, P., What artificial grammar learning reveals about the neurobiology of syntax. Brain and Language 120:2 (2012), 83–95.
67. Pickering, M.J., Garrod, S.C., An integrated theory of language production and comprehension. Behavioral and Brain Sciences, 2013, 1–19.
68. Pickering, M.J., Garrod, S., Self-, other-, and joint monitoring using forward models. Frontiers in Human Neuroscience, 8, 2014, 132.
69. Pope, P.A., Miall, R.C., Task-specific facilitation of cognition by cathodal transcranial direct current stimulation of the cerebellum. Brain Stimulation 5:2 (2012), 84–94.
70. Price, C.J., A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage 62:2 (2012), 816–847.
71. Price, C.J., Devlin, J.T., The interactive account of ventral occipitotemporal contributions to reading. Trends in Cognitive Sciences 15:6 (2011), 246–253.
72. Price, C.J., Mechelli, A., Reading and reading disturbance. Current Opinion in Neurobiology 15:2 (2005), 231–238.
73. Raboyeau, G., Marie, N., Balduyck, S., Gros, H., Démonet, J.-F., Cardebat, D., Lexical learning of the English language: A PET study in healthy French subjects. NeuroImage 22:4 (2004), 1808–1818.
74. Ramnani, N., The primate cortico-cerebellar system: Anatomy and function. Nature Reviews Neuroscience 7:7 (2006), 511–522.
75. Raymond, J.L., Lisberger, S.G., Mauk, M.D., The cerebellum: A neuronal learning machine?. Science 272:5265 (1996), 1126–1131.
76. Riva, D., Giorgi, C., The cerebellum contributes to higher functions during development: Evidence from a series of children surgically treated for posterior fossa tumours. Brain 123:5 (2000), 1051–1061.
77. Rothermich, K., Kotz, S.A., Predictions in speech comprehension: fMRI evidence on the meter-semantic interface. NeuroImage 70 (2013), 89–100.
78. Schlerf, J., Ivry, R.B., Diedrichsen, J., Encoding of sensory prediction errors in the human cerebellum. The Journal of Neuroscience 32:14 (2012), 4913–4922.
79. Schmahmann, J.D., The role of the cerebellum in cognition and emotion: Personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychology Review, 2010, 236–260.
80. Schmahmann, J.D., Sherman, J.C., The cerebellar cognitive affective syndrome. Brain 121:4 (1998), 561–579.
81. Scott, R.B., Stoodley, C.J., Anslow, P., Paul, C., Stein, J.F., Sugden, E.M., et al. Lateralized cognitive deficits in children following cerebellar lesions. Developmental Medicine and Child Neurology 43:10 (2001), 685–691.
82. Shtyrov, Y., Neural bases of rapid word learning. The Neuroscientist 18:4 (2012), 312–319.
83. Shtyrov, Y., Nikulin, V.V., Pulvermüller, F., Rapid cortical plasticity underlying novel word learning. The Journal of Neuroscience 30:50 (2010), 16864–16867.
84. Stoodley, C.J., The cerebellum and cognition: Evidence from functional imaging studies. Cerebellum 11:2 (2012), 352–365.
85. Stoodley, C.J., Schmahmann, J.D., Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. NeuroImage 44:2 (2009), 489–501.
86. Stoodley, C.J., Schmahmann, J.D., The cerebellum and language: Evidence from patients with cerebellar degeneration. Brain and Language 110:3 (2009), 149–153.
87. Stoodley, C.J., Valera, E.M., Schmahmann, J.D., Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. NeuroImage 59:2 (2012), 1560–1570.
88. Strick, P.L., Dum, R.P., Fiez, J.A., Cerebellum and nonmotor function. Annual Review of Neuroscience 32 (2009), 413–434.
89. Thier, P., Dicke, P.W., Haas, R., Thielert, C.-D., Catz, N., The role of the oculomotor vermis in the control of saccadic eye movements. Annals of the New York Academy of Sciences 978 (2002), 50–62.
90. Tian, X., Poeppel, D., Mental imagery of speech and movement implicates the dynamics of internal forward models. Frontiers in Psychology 1 (2010), 1–23.
91. Timmann, D., Drepper, J., Frings, M., Maschke, M., Richter, S., Gerwig, M., et al. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex 46:7 (2010), 845–857.
92. Tse, D., Langston, R.F., Kakeyama, M., Bethus, I., Spooner, P.A, Wood, E.R., et al. Schemas and memory consolidation. Science (New York, N.Y.) 316:April (2007), 76–82.
93. Twomey, T., Kawabata Duncan, K.J., Price, C.J., Devlin, J.T., Top-down modulation of ventral occipito-temporal responses during visual word recognition. NeuroImage 55:3 (2011), 1242–1251.
94. Vandenberghe, R., Price, C.J., Wise, R., Josephs, O., Frackowiak, R., Functional anatomy of a common semantic system for words and pictures. Nature 383 (1996), 254–256.
95. Verstynen, T.D., Deshpande, V., Using pulse oximetry to account for high and low frequency physiological artifacts in the BOLD signal. NeuroImage 55:4 (2011), 1633–1644.
96. Wolpert, D.M., Miall, R.C., Forward models for physiological motor control. Neural Networks 9:8 (1996), 1265–1279.
97. Wolpert, D.M., Miall, R.C., Kawato, M., Internal models in the cerebellum. Trends in Cognitive Sciences 2:9 (1998), 338–347.