Unconscious learning versus visual perception: Dissociable roles for gamma oscillations revealed in MEG

Journal of Cognitive Neuroscience

Volumn 21, Issue 12, 2009, Pages 2287-2299

  Chaumon, Maximilien ^a   Schwartz, Denis ^b   Tallon Baudry, Catherine ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; EVOKED RESPONSE; EXPLICIT MEMORY; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MAGNETOENCEPHALOGRAPHY; MALE; NERVE CELL NETWORK; NORMAL HUMAN; OSCILLATION; PRIORITY JOURNAL; VISION;

ADULT; ATTENTION; BIOLOGICAL CLOCKS; BRAIN; BRAIN MAPPING; COLOR PERCEPTION; CUES; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; LEARNING; MAGNETOENCEPHALOGRAPHY; MALE; ORIENTATION; PHOTIC STIMULATION; REACTION TIME; TIME FACTORS; UNCONSCIOUS (PSYCHOLOGY); YOUNG ADULT;

EID: 70350435442     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn.2008.21155     Document Type: Article

References (71)

1. Abbott, L. F., & Nelson, S. B. (2000). Synaptic plasticity: Taming the beast. Nature Neuroscience, 3 (Suppl.), 1178-1183.
2. Ahissar, M., & Hochstein, S. (2004). The reverse hierarchy theory of visual perceptual learning. Trends in Cognitive Sciences, 8, 457-464. (Pubitemid 39265449)
3. Bar, M. (2004). Visual objects in context. Nature Reviews Neuroscience, 5, 617-629.
4. Bar, M., Kassam, K. S., Ghuman, A. S., Boshyan, J., Schmidt, A. M., Dale, A. M., et al. (2006). Top-down facilitation of visual recognition. Proceedings of the National Academy of Sciences, U.S.A., 103, 449-454.
5. Bauer, E. P., Paz, R., & Pare, D. (2007). Gamma oscillations coordinate amygdalo-rhinal interactions during learning. Journal of Neuroscience, 27, 9369-9379. (Pubitemid 47358215)
6. Bi, G.-Q., & Poo, M.-M. (1998). Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience, 18, 10464-10472.
7. Bi, G.-Q., & Rubin, J. (2005). Timing in synaptic plasticity: From detection to integration. Trends in Neurosciences, 28, 222-228.
8. Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995). Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. Journal of Neuroscience, 15, 47-60.
9. Brainard, D. H. (1997). The Psychophysics Toolbox. Spatial Vision, 10, 433-436.
10. Burgess, N., Maguire, E. A., & O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35, 625-641. (Pubitemid 35223024)
11. Chaumon, M., Drouet, V., & Tallon-Baudry, C. (2008). Unconscious associative memory affects visual processing before 100 ms. Journal of Vision, 8, 1-10.
12. Chun, M. M., & Jiang, Y. (1998). Contextual cueing: Implicit learning and memory of visual context guides spatial attention. Cognitive Psychology, 36, 28-71.
13. Chun, M. M., & Jiang, Y. (2003). Implicit, long-term spatial contextual memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 29, 224-234.
14. Csicsvari, J., Jamieson, B., Wise, K. D., & Buzsaki, G. (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron, 37, 311-322. (Pubitemid 36143825)
15. Dan, Y., & Poo, M.-M. (2004). Spike timing-dependent plasticity of neural circuits. Neuron, 44, 23-30. (Pubitemid 39348828)
16. Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proceedings of the National Academy of Sciences, U.S.A., 93, 13494-13499.
17. Fell, J., Klaver, P., Lehnertz, K., Grunwald, T., Schaller, C., Elger, C. E., et al. (2001). Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nature Neuroscience, 4, 1259-1264. (Pubitemid 33135633)
18. Fiebach, C. J., Gruber, T., & Supp, G. G. (2005). Neuronal mechanisms of repetition priming in occipitotemporal cortex: Spatiotemporal evidence from functional magnetic resonance imaging and electroencephalography. Journal of Neuroscience, 25, 3414-3422. (Pubitemid 40471349)
19. Fries, P., Reynolds, J. H., Rorie, A. E., & Desimone, R. (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science, 291, 1560-1563. (Pubitemid 32179225)
20. Gonzalez Andino, S. L., Michel, C. M., Thut, G., Landis, T., & Grave de Peralta, R. (2005). Prediction of response speed by anticipatory high-frequency (gamma band) oscillations in the human brain. Human Brain Mapping, 24, 50-58.
21. Gratton, G., Coles, M. G., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55, 468-484.
22. Greene, A. J., Gross, W. L., Elsinger, C. L., & Rao, S. M. (2007). Hippocampal differentiation without recognition: An fMRI analysis of the contextual cueing task. Learning and Memory, 14, 548-553.
23. Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: Neural models of stimulus-specific effects. Trends in Cognitive Sciences, 10, 14-23. (Pubitemid 43049768)
24. Gruber, T., Keil, A., & Müller, M. M. (2001). Modulation of induced gamma band responses and phase synchrony in a paired associate learning task in the human EEG. Neuroscience Letters, 316, 29-32. (Pubitemid 33092026)
25. Gruber, T., & Müller, M. M. (2002). Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG. Brain Research, Cognitive Brain Research, 13, 377-392. (Pubitemid 34252968)
26. Gruber, T., & Müller, M. M. (2005). Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. Cerebral Cortex, 15, 109-116. (Pubitemid 40019056)
27. Gruber, T., & Müller, M. M. (2006). Oscillatory brain activity in the human EEG during indirect and direct memory tasks. Brain Research, 1097, 194-204. (Pubitemid 44041291)
28. Gruber, T., Müller, M. M., Keil, A., & Elbert, T. (1999). Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clinical Neurophysiology, 110, 2074-2085. (Pubitemid 29528404)
29. Gruber, T., Trujillo-Barreto, N. J., Giabbiconi, C. M., Valdes-Sosa, P. A., & Müller, M. M. (2006). Brain electrical tomography (BET) analysis of induced gamma band responses during a simple object recognition task. Neuroimage, 29, 888-900. (Pubitemid 43124050)
30. Gruber, T., Tsivilis, D., Montaldi, D., & Müller, M. M. (2004). Induced gamma band responses: An early marker of memory encoding and retrieval. NeuroReport, 15, 1837-1841. (Pubitemid 39062605)
31. Hebb, D. O. (1949). The organization of behavior: A neuropsychological theory (2002 ed.). Mahwah, NJ: Erlbaum.
32. Herrmann, C. S., Munk, M. H., & Engel, A. K. (2004). Cognitive functions of gamma-band activity: Memory match and utilization. Trends in Cognitive Sciences, 8, 347-355.
33. Hochstein, S., & Ahissar, M. (2002). View from the top: Hierarchies and reverse hierarchies in the visual system. Neuron, 36, 791-804. (Pubitemid 35447852)
34. Hoogenboom, N., Schoffelen, J. M., Oostenveld, R., Parkes, L. M., & Fries, P. (2006). Localizing human visual gamma-band activity in frequency, time and space. Neuroimage, 29, 764-773. (Pubitemid 43121201)
35. Jensen, O., Kaiser, J., & Lachaux, J. P. (2007). Human gamma-frequency oscillations associated with attention and memory. Trends in Neurosciences, 30, 317-324. (Pubitemid 46991117)
36. Jiang, Y., Song, J., & Rigas, A. (2005). High-capacity spatial contextual memory. Psychonomic Bulletin & Review, 12, 524-529.
37. Kaiser, J., Buhler, M., & Lutzenberger, W. (2004). Magnetoencephalographic gamma-band responses to illusory triangles in humans. Neuroimage, 23, 551-560. (Pubitemid 39370606)
38. Kiebel, S. J., Tallon-Baudry, C., & Friston, K. J. (2005). Parametric analysis of oscillatory activity as measured with EEG/MEG. Human Brain Mapping, 26, 170-177. (Pubitemid 41598315)
39. Lachaux, J.-P., Rodriguez, E., Martinerie, J., & Varela, F. J. (1999). Measuring phase synchrony in brain signals. Human Brain Mapping, 8, 194-208.
40. Lau, H. C., & Passingham, R. E. (2007). Unconscious activation of the cognitive control system in the human prefrontal cortex. Journal of Neuroscience, 27, 5805-5811. (Pubitemid 350021086)
41. Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213-215. (Pubitemid 27034762)
42. Melloni, L., Molina, C., Pena, M., Torres, D., Singer, W., & Rodriguez, E. (2007). Synchronization of neural activity across cortical areas correlates with conscious perception. Journal of Neuroscience, 27, 2858-2865. (Pubitemid 46438979)
43. Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167-202. (Pubitemid 32695227)
44. Miltner, W. H., Braun, C., Arnold, M., Witte, H., & Taub, E. (1999). Coherence of gamma-band EEG activity as a basis for associative learning. Nature, 397, 434-436. (Pubitemid 29078910)
45. Montgomery, S. M., & Buzsaki, G. (2007). Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proceedings of the National Academy of Sciences, U.S.A., 104, 14495-14500.
46. Neumann, O., & Klotz, W. (1994). Motor responses to nonreportable, masked stimuli: Where is the limit of direct parameter specification? In C. Umiltà & M. Moscovitch (Eds.), Conscious and nonconscious information processing (Vol. XV, pp. 123-150). Cambridge, MA: MIT Press.
47. Oliva, A. (2005). Gist of the scene. In L. Itti, G. Rees, & J. K. Tsotsos (Eds.), The encyclopedia of neurobiology of attention (pp. 251-256). San Diego, CA: Elsevier.
48. Oliva, A., & Schyns, P. G. (1997). Coarse blobs or fine edges? Evidence that information diagnosticity changes the perception of complex visual stimuli. Cognitive Psychology, 34, 72-107. (Pubitemid 127372040)
49. Osipova, D., Takashima, A., Oostenveld, R., Fernandez, G., Maris, E., & Jensen, O. (2006). Theta and gamma oscillations predict encoding and retrieval of declarative memory. Journal of Neuroscience, 26, 7523-7531. (Pubitemid 44315221)
50. Rodriguez, R., Kallenbach, U., Singer, W., & Munk, M. H. J. (2004). Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. Journal of Neuroscience, 24, 10369-10378. (Pubitemid 39552621)
51. Rose, M., Haider, H., & Büchel, C. (2005). Unconscious detection of implicit expectancies. Journal of Cognitive Neuroscience, 17, 918-927.
52. Ross, R. S., & Slotnick, S. D. (2008). The hippocampus is preferentially associated with memory for spatial context. Journal of Cognitive Neuroscience, 20, 432-446. (Pubitemid 351317602)
53. Schurger, A., Cowey, A., & Tallon-Baudry, C. (2006). Induced gamma-band oscillations correlate with awareness in hemianopic patient GY. Neuropsychologia, 44, 1796-1803. (Pubitemid 43928005)
54. Sederberg, P. B., Kahana, M. J., Howard, M. W., Donner, E. J., & Madsen, J. R. (2003). Theta and gamma oscillations during encoding predict subsequent recall. Journal of Neuroscience, 23, 10809-10814.
55. Sederberg, P. B., Schulze-Bonhage, A., Madsen, J. R., Bromfield, E. B., McCarthy, D. C., Brandt, A., et al. (2007). Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cerebral Cortex, 17, 1190-1196. (Pubitemid 46598861)
56. Sejnowski, T. J., & Paulsen, O. (2006). Network oscillations: Emerging computational principles. Journal of Neuroscience, 26, 1673-1676.
57. Singer, W. (1995). Development and plasticity of cortical processing architectures. Science, 270, 758-764.
58. Singer, W. (1999). Time as coding space? Current Opinion in Neurobiology, 9, 189-194.
59. Smyth, A. C., & Shanks, D. R. (2008). Awareness in contextual cuing with extended and concurrent explicit tests. Memory & Cognition, 36, 403-415.
60. Stiefel, K. M., Tennigkeit, F., & Singer, W. (2005). Synaptic plasticity in the absence of backpropagating spikes of layer II inputs to layer V pyramidal cells in rat visual cortex. European Journal of Neuroscience, 21, 2605-2610. (Pubitemid 40813943)
61. Summerfield, C., & Mangels, J. A. (2006). Dissociable neural mechanisms for encoding predictable and unpredictable events. Journal of Cognitive Neuroscience, 18, 1120-1132. (Pubitemid 44066116)
62. Supp, G. G., Schlögl, A., Trujillo-Barreto, N., Müller, M. M., & Gruber, T. (2007). Directed cortical information flow during human object recognition: Analyzing induced EEG gamma-band responses in brain's source space. PLoS ONE, 2, e684.
63. Tallon-Baudry, C., & Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends in Cognitive Sciences, 3, 151-162. (Pubitemid 29155465)
64. Tallon-Baudry, C., Bertrand, O., Delpuech, C., & Pernier, J. (1997). Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. Journal of Neuroscience, 17, 722-734. (Pubitemid 27024584)
65. Tallon-Baudry, C., Bertrand, O., Delpuech, C., & Pernier, J. (1996). Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. Journal of Neuroscience, 16, 4240-4249. (Pubitemid 26192419)
66. Tallon-Baudry, C., Bertrand, O., & Fischer, C. (2001). Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. Journal of Neuroscience, 21, RC177.
67. VanRullen, R. (2003). Visual saliency and spike timing in the ventral visual pathway. Journal of Physiology Paris, 97, 365-377. (Pubitemid 38177333)
68. Vidal, J. R., Chaumon, M., O'Regan, J. K., & Tallon-Baudry, C. (2006). Visual grouping and the focusing of attention induce gamma-band oscillations at different frequencies in human magnetoencephalogram signals. Journal of Cognitive Neuroscience, 18, 1850-1862. (Pubitemid 44674284)
69. Wespatat, V., Tennigkeit, F., & Singer, W. (2004). Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex. Journal of Neuroscience, 24, 9067-9075. (Pubitemid 39372250)
70. Wiggs, C. L., & Martin, A. (1998). Properties and mechanisms of perceptual priming. Current Opinion in Neurobiology, 8, 227-233.
71. Wyart, V., & Tallon-Baudry, C. (2008). Neural dissociation between visual awareness and spatial attention. Journal of Neuroscience, 28, 2667-2679. (Pubitemid 351348208)