Early visual learning induces long-lasting connectivity changes during rest in the human brain

NeuroImage

Volumn 77, Issue , 2013, Pages 148-156

  Urner, Maren ^a,b   Schwarzkopf, Dietrich Samuel ^a,b   Friston, Karl ^b   Rees, Geraint ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Early learning; FMRI; Hippocampus; Resting state connectivity; Stochastic DCM; Striatum

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; CELL ACTIVITY; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MENTAL TASK; MOVEMENT PERCEPTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NEUROPHYSIOLOGY; NORMAL HUMAN; PARIETAL CORTEX; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; RESTING STATE; SENSORY ANALYSIS; STOCHASTIC MODEL; VISUAL CORTEX; VISUAL INFORMATION; VISUAL LEARNING;

ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; NEURONAL PLASTICITY; REST; TIME FACTORS; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84876713760     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.03.050     Document Type: Article

References (74)

1. Adab H.Z., Vogels R. Practicing coarse orientation discrimination improves orientation signals in macaque cortical area V4. Curr. Biol. 2011, 21:1661-1666.
2. Albert N.B., Robertson E.M., Miall R.C. The resting human brain and motor learning. Curr. Biol. 2009, 19:1023-1027.
3. Baker C.L., Hess R.F., Zihl J. Residual motion perception in a "motion-blind" patient, assessed with limited-lifetime random dot stimuli. J. Neurosci. 1991, 11:454-461.
4. Baldassarre A., Lewis C.M., Committeri G., Snyder A.Z. Individual variability in functional connectivity predicts performance of a perceptual task. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3516-3521.
5. Battaglia F.P., Benchenane K., Sirota A., Pennartz C.M.A., Wiener S.I. The hippocampus: hub of brain network communication for memory. Trends Cogn. Sci. 2011, 15:310-318.
6. Birn R.M. The behavioral significance of spontaneous fluctuations in brain activity. Neuron 2007, 56:8-9.
7. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
8. Blakemore B.C., Campbell F.W. On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol. 1969, 203:237-260.
9. Brovelli A., Laksiri N., Nazarian B., Meunier M., Boussaoud D. Understanding the neural computations of arbitrary visuomotor learning through fMRI and associative learning theory. Cereb. Cortex 2008, 18:1485-1495.
10. Buckley M.J. The role of the perirhinal cortex and hippocampus in learning, memory, and perception. Q. J. Exp. Psychol. B 2005, 58:246-268.
11. Colgin L.L., Moser E.I., Moser M.-B. Understanding memory through hippocampal remapping. Trends Neurosci. 2008, 31:469-477.
12. Cowey A., Marcar V.L. The effect of removing superior temporal cortical motion areas in the macaque monkey: I. Motion discrimination using simple dots. Eur. J. Neurosci. 1992, 4:1219-1227.
13. Damoiseaux J.S., Rombouts S.A.R.B., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
14. Ding L., Gold J.I. Caudate encodes multiple computations for perceptual decisions. J. Neurosci. 2010, 30:15747-15759.
15. Dudai Y. The restless engram: consolidations never end. Annu. Rev. Neurosci. 2012, 35:227-247.
16. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 2005, 25:1325-1335.
17. Fiorentini A., Berardi N. Learning in grating waveform discrimination: specificity for orientation and spatial frequency. Vis. Res. 1981, 21:1149-1158.
18. Forkstam C., Petersson K.M. Towards an explicit account of implicit learning. Curr. Opin. Neurol. 2005, 18:435-441.
19. Fortin N.J., Agster K.L., Eichenbaum H.B. Critical role of the hippocampus in memory for sequences of events. Nat. Neurosci. 2002, 5:458-462.
20. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
21. Frensch P.A., Runger D. Implicit learning. Curr. Dir. Psychol. Sci. 2003, 12:13-18.
22. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 1997, 6:218-229.
23. Fukunaga M., Horovitz S.G., Van Gelderen P., De Zwart J.A., Jansma J.M., Ikonomidou V.N., Chu R., Deckers R.H.R., Leopold D.A., Duyn J.H. Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. Magn. Reson. Imaging 2006, 24:979-992.
24. Gheysen F., Van Opstal F., Roggeman C., Van Waelvelde H., Fias W. The neural basis of implicit perceptual sequence learning. Front. Hum. Neurosci. 2011, 5:137.
25. Glover G.H., Li T.Q., Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000, 44:162-167. (official journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine).
26. Goldstone R.L. Perceptual learning. Annu. Rev. Psychol. 1998, 49:585-612.
27. Graham K.S., Scahill V.L., Hornberger M., Barense M.D., Lee A.C.H., Bussey T.J., Saksida L.M. Abnormal categorization and perceptual learning in patients with hippocampal damage. J. Neurosci. 2006, 26:7547-7554.
28. Hasson U., Nusbaum H.C., Small S.L. Task-dependent organization of brain regions active during rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:10841-10846.
29. Hutton C., Josephs O., Stadler J., Featherstone E., Reid A., Speck O., Bernarding J., Weiskopf N. The impact of physiological noise correction on fMRI at 7 T. NeuroImage 2011, 57:101-112.
30. Kahnt T., Grueschow M., Speck O., Haynes J.-D. Perceptual learning and decision-making in human medial frontal cortex. Neuron 2011, 70:549-559.
31. Law C.-T., Gold J.I. Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area. Nat. Neurosci. 2008, 11:505-513.
32. Law C., Gold J.I. Reinforcement learning can account for associative and perceptual learning on a visual decision task. Nat. Neurosci. 2009, 12:655-663.
33. Lee A.C.H., Bussey T.J., Murray E.A., Saksida L.M., Epstein R.A., Kapur N., Hodges J.R., Graham K.S. Perceptual deficits in amnesia: challenging the medial temporal lobe "mnemonic" view. Neuropsychologia 2005, 43:1-11.
34. Lewis C.M., Baldassarre A., Committeri G., Romani G.L., Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17558-17563.
35. Li B., Daunizeau J., Stephan K.E., Penny W., Hu D., Friston K. Generalised filtering and stochastic DCM for fMRI. NeuroImage 2011, 58:442-457.
36. 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. J. Cogn. Neurosci. 2004, 16:427-438.
37. Mathews R., Buss R., Stanley W., Fields B., Cho J., Bruhan B. Role of implicit and explicit processes of learning from examples: a synergistic effect. J. Exp. Psychol. Learn. Mem. Cogn. 1989, 15:1083-1100.
38. May A. Experience-dependent structural plasticity in the adult human brain. Trends Cogn. Sci. 2011, 15:475-482.
39. Meindl T., Teipel S., Elmouden R., Mueller S., Koch W., Dietrich O., Coates U., Reiser M., Glaser C. Test-retest reproducibility of the default-mode network in healthy individuals. Hum. Brain Mapp. 2010, 31:237-246.
40. Neves G., Cooke S.F., Bliss T.V.P. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 2008, 9:65-75.
41. Newsome W.T., Salzman C.D. The neuronal basis of motion perception. CIBA Found. Symp. 1993, 174:217-230. (discussion 230-46).
42. Packard M.G., Knowlton B.J. Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 2002, 25:563-593.
43. Penfield W., Milner B. Memory deficit produced by bilateral lesions in the hippocampal zone. A.M.A. Arch. Neurol. Psychiatry 1958, 79:475-497.
44. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
45. Raichle M.E. Two views of brain function. Trends Cogn. Sci. 2010, 14:180-190.
46. Reber A.S. Implicit learning and tacit knowledge. J. Exp. Psychol. Gen. 1989, 118:219-235.
47. Rees G., Friston K., Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 2000, 3:716-723.
48. Reiss J.P., Campbell D.W., Leslie W.D., Paulus M.P., Stroman P.W., Polimeni J.O., Malcolmson K.A., Sareen J. The role of the striatum in implicit learning: a functional magnetic resonance imaging study. Neuroreport 2005, 16:1291-1295.
49. Rose M., Haider H., Salari N., Büchel C. Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. J. Neurosci. 2011, 31:13739-13745.
50. Schapiro A.C., Kustner L.V., Turk-Browne N.B. Shaping of object representations in the human medial temporal lobe based on temporal regularities. Curr. Biol. 2012, 22:1622-1627.
51. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003, 37:1013-1025.
52. Schölvinck M.L., Friston K.J., Rees G. The influence of spontaneous activity on stimulus processing in primary visual cortex. NeuroImage 2012, 59:2700-2708.
53. Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 2007, 30:259-288.
54. Seitz A., Watanabe T. A unified model for perceptual learning. Trends Cogn. Sci. 2005, 9:329-334.
55. Seitz A.R., Yamagishi N., Werner B., Goda N., Kawato M., Watanabe T. Task-specific disruption of perceptual learning. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14895-14900.
56. Shibata K., Watanabe T., Sasaki Y., Kawato M. Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation. Science 2011, 334:1413-1415.
57. Shtyrov Y. Neural bases of rapid word learning. Neuroscientist 2012, 18:312-319.
58. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
59. Stevens W.D., Buckner R.L., Schacter D.L. Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. Cereb. Cortex 2010, 20:1997-2006.
60. Sun R., Thomas M., McClelland J., Griffiths T., Kemp C., Tenenbaum J., Schoener G., Bringsjord S., Taatgen N., Anderson J., Norman K., Detre G., Polyn S., Rogers T., Kruschke J., Busemeyer J., Johnson J., Heit E., Johnson-Laird P., Yang Y., Cleeremans A., Dienes Z., Pisapia N.De, Repovs G., Braver T., Shultz T., Sirois S., Chater N., Christiansen M., Read S., Monroe B., Thagard P., Litt A., Gray W., Lopez F., Shanks D., Sinha P., Balas B., Mussa-Ivaldi F., Solla S. The Cambridge Handbook of Computational Psychology 2008, Cambridge University Press, Cambridge.
61. Sutton R., Barto A. Reinforcement Learning: An Introduction 1998, MIT Press, Cambridge, Mass.
62. Tadin D., Silvanto J., Pascual-Leone A., Battelli L. Improved motion perception and impaired spatial suppression following disruption of cortical area MT/V5. J. Neurosci. 2011, 31:1279-1283.
63. Tambini A., Ketz N., Davachi L. Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 2010, 65:280-290.
64. Turk-Browne N.B., Scholl B.J., Johnson M.K., Chun M.M. Implicit perceptual anticipation triggered by statistical learning. J. Neurosci. 2010, 30:11177-11187.
65. Vaina L.M., Sundareswaran V., Harris J.G. Learning to ignore: psychophysics and computational modeling of fast learning of direction in noisy motion stimuli. Brain Res. Cogn. Brain Res. 1995, 2:155-163.
66. Vaina L.M., Belliveau J.W., Des Roziers E.B., Zeffiro T.A. Neural systems underlying learning and representation of global motion. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12657-12662.
67. Vaina L.M., Cowey A., Eskew R.T., LeMay M., Kemper T. Regional cerebral correlates of global motion perception: evidence from unilateral cerebral brain damage. Brain 2001, 124:310-321.
68. Van Opstal F., Verguts T., Orban G.A., Fias W. A hippocampal-parietal network for learning an ordered sequence. NeuroImage 2008, 40:333-341.
69. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
70. Walsh V., Ellison A., Ashbridge E., Cowey A. The role of the parietal cortex in visual attention-hemispheric asymmetries and the effects of learning: a magnetic stimulation study. Neuropsychologia 1999, 37:245-251.
71. Wang G., Grone B., Colas D., Appelbaum L., Mourrain P. Synaptic plasticity in sleep: learning, homeostasis and disease. Trends Neurosci. 2011, 34:452-463.
72. Wilkinson L., Jahanshahi M. The striatum and probabilistic implicit sequence learning. Brain Res. 2007, 1137:117-130.
73. Winocur G. The hippocampus and thalamus: their roles in short- and long-term memory and the effects of interference. Behav. Brain Res. 1985, 16:135-152.
74. Zuo X.-N., Kelly C., Adelstein J.S., Klein D.F., Castellanos F.X., Milham M.P. Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. NeuroImage 2010, 49:2163-2177.