Neural dynamics associated with semantic and episodic memory for faces: Evidence from multiple frequency bands

Journal of Cognitive Neuroscience

Volumn 22, Issue 2, 2010, Pages 263-277

  Zion Golumbic, Elana ^a   Kutas, Marta ^b   Bentin, Shlomo ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; CONTROLLED STUDY; DYNAMICS; EPISODIC MEMORY; FACE; FEMALE; GAMMA RHYTHM; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY CONSOLIDATION; NORMAL HUMAN; PRIORITY JOURNAL; RECALL; RECOGNITION; SEMANTIC MEMORY; TASK PERFORMANCE; THETA RHYTHM;

ADULT; ASSOCIATION; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; FACE; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; NEUROPSYCHOLOGICAL TESTS; NONLINEAR DYNAMICS; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REACTION TIME; RECOGNITION (PSYCHOLOGY); SEMANTICS; YOUNG ADULT;

EID: 75749085781     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn.2009.21251     Document Type: Article

References (107)

1. Allport, D. A. (1985). Distributed memory, modular subsystems and dysphasia. In S. K. Newman & R. Epstein (Eds.), Current perspectives in dysphasia (pp. 32-60). Edinburgh: Churchill Livingstone.
2. Anaki, D., Zion-Golumbic, E., & Bentin, S. (2007). Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces. Neuroimage, 37, 1407-1416.
3. Axmacher, N., Elger, C. E., & Fell, J. (2008). Memory formation by refinement of neural representations: The inhibition hypothesis. Behavioural Brain Research, 189, 1-8.
4. Brown, M. W., & Xiang, J. Z. (1998). Recognition memory: Neuronal substrates of the judgement of prior occurrence. Progress in Neurobiology, 55, 149-189.
5. Burgess, A. P., & Gruzelier, J. H. (1997). Short duration synchronization of human theta rhythm during recognition memory. NeuroReport, 8, 1039-1042.
6. Burgess, A. P., & Gruzelier, J. H. (2000). Short duration power changes in the EEG during recognition memory for words and faces. Psychophysiology, 37, 596-606.
7. Buzsáki, G. (2002). Theta oscillations in the hippocampus. Neuron, 33, 325-340.
8. Buzsáki, G. (2005). Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory. Hippocampus, 15, 827-840.
9. Buzsáki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304, 1926-1929.
10. Coltheart, M., Inglis, L., Cupples, L., Michie, P., Bates, A., & Budd, B. (1998). A semantic subsystem of visual attributes. Neurocase, 4, 353-370.
11. Craik, F. I. (2002). Levels of processing: Past, present, and future? Memory, 10, 305-318.
12. Craik, F. I., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11, 671-684.
13. Craik, F. I., & Tulving, E. (1975). Depth of processing and the retention of words in episodic memory. Journal of Experimental Psychology: General, 104, 268-294.
14. Doppelmayr, M., Klimesch, W., Hödlmoser, K., Sauseng, P., & Gruber, W. (2005). Intelligence related upper alpha desynchronization in a semantic memory task. Brain Research Bulletin, 66, 171-177.
15. Doppelmayr, M., Klimesch, W., Schwaiger, J., Auinger, P., & Winkler, T. (1998). Theta synchronization in the human EEG and episodic retrieval. Neuroscience Letters, 257, 41-44.
16. Doppelmayr, M., Klimesch, W., Schwaiger, J., Stadler, W., & Röhm, D. (2000). The time locked theta response reflects interindividual differences in human memory performance. Neuroscience Letters, 278, 141-144.
17. Düzel, E., Habib, R., Guderian, S., & Heinze, H. J. (2004). Four types of novelty-familiarity responses in associative recognition memory of humans. European Journal of Neuroscience, 19, 1408-1416.
18. Düzel, E., Neufang, M., & Heinze, H. J. (2005). The oscillatory dynamics of recognition memory and its relationship to event-related responses. Cerebral Cortex, 15, 1992-2000.
19. Eimer, M. (2000). Event-related brain potentials distinguish processing stages involved in face perception and recognition. Clinical Neurophysiology, 111, 694-705.
20. Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic predictions: Oscillations and synchrony in top-down processing. Nature Reviews Neuroscience, 2, 704-716.
21. Fell, J., Klaver, P., Elfadil, H., Schaller, C., Elger, C. E., & Fernández, G. (2003). Rhinal-hippocampal theta coherence during declarative memory formation: Interaction with gamma synchronization? European Journal of Neuroscience, 17, 1082-1088.
22. 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.
23. Freunberger, R., Klimesch, W., Griesmayr, B., Sauseng, P., & Gruber, W. (2008). Alpha phase coupling reflects object recognition. Neuroimage, 42, 928-935.
24. Fries, P. (2005). A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends in Cognitive Sciences, 9, 474-480.
25. Fries, P., Nikolí, D., & Singer, W. (2007). The gamma cycle. Trends in Cognitive Sciences, 30, 309-316.
26. Fries, P., Schröder, J. H., Roelfsema, P. R., Singer, W., & Engel, A. K. (2002). Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection. Journal of Neuroscience, 22, 3739-3754.
27. Fuster, J. M. (1995). Memory in the cerebral cortex: An empirical approach to neural networks in the human and nonhuman. Cambridge, MA: MIT Press.
28. Gainotti, G., Silveri, M. C., Daniele, A., & Giustolisi, L. (1995). Neuroanatomical correlates of category-specific semantic disorders: A critical survey. Memory, 3, 247-264.
29. Gobbini, M. I., & Haxby, J. V. (2006). Neural systems for recognition of familiar faces. Neuropsychologia, 45, 32-41.
30. Greenstein, Y. J., Pavlides, C., & Winson, J. (1988). Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Research, 438, 331-334.
31. Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., & Malach, R. (1999). Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron, 24, 187-203.
32. Gruber, T., Maess, B., Trujillo-Barreto, N. J., & Müller, M. M. (2008). Sources of synchronized induced gamma-band responses during a simple object recognition task: A replication study in human MEG. Brain Research, 1196, 74-84.
33. Gruber, T., & Müller, M. M. (2002). Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG. Cognitive Brain Research, 13, 377-392.
34. 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.
35. Gruber, T., Tsivilis, D., Giabbiconi, C. M., & Müller, M. M. (2008). Induced electroencephalogram oscillations during source memory: Familiarity is reflected in the gamma band, recollection in the theta band. Journal of Cognitive Neuroscience, 20, 1043-1053.
36. Gruber, W. R., Klimesch, W., Sauseng, P., & Doppelmayr, M. (2005). Alpha phase synchronization predicts P1 and N1 latency and amplitude size. Cerebral Cortex, 15, 371-377.
37. Halberstadt, J. (2006). The generality and ultimate origins of the attractiveness of prototypes. Personality and Social Psychology Review, 10, 166-183.
38. Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223-233.
39. Henson, R. N., Goshen-Gottstein, Y., Ganel, T., Otten, L. J., Quayle, A., & Rugg, M. D. (2003). Electrophysiological and haemodynamic correlates of face perception, recognition and priming. Cerebral Cortex, 13, 793-805.
40. Henson, R. N., & Rugg, M. D. (2003). Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia, 41, 263-270.
41. Howard, M. W., Rizzuto, D. S., Caplan, J. B., Madsen, J. R., Lisman, J., Aschenbrenner-Scheibe, R., et al. (2003). Gamma oscillations correlate with working memory load in humans. Cerebral Cortex, 13, 1369-1374.
42. Jackson, M. C., & Raymond, J. E. (2006). The role of attention and familiarity in face identification. Perception & Psychophysics, 68, 543-557.
43. Jacobs, J., Kahana, M. J., Ekstrom, A. D., & Fried, I. (2007). Brain oscillations control timing of single-neuron activity in humans. Journal of Neuroscience, 27, 3839-3844.
44. Jensen, O., Kaiser, J., & Lachaux, J. P. (2007). Human gamma-frequency oscillations associated with attention and memory. Trends in Neurosciences, 30, 317-324.
45. Jeschke, M., Lenz, D., Budinger, E., Herrmann, C. S., & Ohl, F. W. (2008). Gamma oscillations in gerbil auditory cortex during a target-discrimination task reflect matches with short-term memory. Brain Research, 1220, 70-80.
46. Jokisch, D., & Jensen, O. (2007). Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. Journal of Neuroscience, 27, 3244-3251.
47. Kahana, M. J., Seelig, D., & Madsen, J. R. (2001). Theta returns. Current Opinion in Neurobiology, 11, 739-744.
48. Kellenbach, M. L., Brett, M., & Patterson, K. (2001). Large, colorful, or noisy? Attribute- and modality-specific activations during retrieval of perceptual attribute knowledge. Cognitive, Affective & Behavioral Neuroscience, 3, 207-221.
49. Kirk, I. J., & Mackay, J. C. (2003). The role of theta-range oscillations in synchronising and integrating activity in distributed mnemonic networks. Cortex, 39, 993-1008.
50. Klimesch, W., Doppelmayr, M., & Hanslmayr, S. (2006). Upper alpha ERD and absolute power: Their meaning for memory performance. Progress in Brain Research, 159, 151-165.
51. Klimesch, W., Doppelmayr, M., Pachinger, T., & Ripper, B. (1997). Brain oscillations and human memory: EEG correlates in the upper alpha and theta band. Neuroscience Letters, 238, 9-12.
52. Klimesch, W., Doppelmayr, M., Pachinger, T., & Russegger, H. (1997). Event-related desynchronization in the alpha band and the processing of semantic information. Cognitive Brain Research, 6, 83-94.
53. Klimesch, W., Doppelmayr, M., Schimke, H., & Ripper, B. (1997). Theta synchronization and alpha desynchronization in a memory task. Psychophysiology, 34, 169-176.
54. Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53, 63-88.
55. Klimesch, W., Schimke, H., & Schwaiger, J. (1994). Episodic and semantic memory: An analysis in the EEG theta and alpha band. Electroencephalography and Clinical Neurophysiology, 91, 428-441.
56. Lachaux, J. P., Fonlupt, P., Kahane, P., Minotti, L., Hoffmann, D., Bertrand, O., et al. (2007). Relationship between task-related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG. Human Brain Mapping, 28, 1368-1375.
57. Lachaux, J. P., George, N., Tallon-Baudry, C., Martinerie, J., Hugueville, L., Minotti, L., et al. (2005). The many faces of the gamma band response to complex visual stimuli. Neuroimage, 25, 491-501.
58. Larson, J., Wong, D., & Lynch, G. (1986). Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Research, 368, 347-350.
59. Lenz, D., Jeschke, M., Schadow, J., Naue, N., Ohl, F. W., & Herrmann, C. S. (2008). Human EEG very high frequency oscillations reflect the number of matches with a template in auditory short-term memory. Brain Research, 1220, 81-92.
60. Leube, D. T., Erb, M., Grodd, W., Bartels, M., & Kircher, T. T. (2003). Successful episodic memory retrieval of newly learned faces activates a left fronto-parietal network. Cognitive Brain Research, 18, 97-101.
61. Leveroni, C. L., Seidenberg, M., Mayer, A. R., Mead, L. A., Binder, J. R., & Rao, S. M. (2000). Neural systems underlying the recognition of familiar and newly learned faces. Journal of Neuroscience, 20, 878-886.
62. Li, L., Miller, E. K., & Desimone, R. (1993). The representation of stimulus familiarity in anterior inferior temporal cortex. Journal of Neurophysiology, 69, 1918-1929.
63. Lutzenberger, W., Pulvermüller, F., Elbert, T., & Birbaumer, N. (1995). Visual stimulation alters local 40-Hz responses in humans: An EEG-study. Neuroscience Letters, 183, 39-42.
64. Mainy, N., Kahane, P., Minotti, L., Hoffmann, D., Bertrand, O., & Lachaux, J. P. (2007). Neural correlates of consolidation in working memory. Human Brain Mapping, 28, 183-193.
65. Makeig, S., Westerfield, M., Jung, T. P., Enghoff, S., Townsend, J., Courchesne, E., et al. (2002). Dynamic brain sources of visual evoked responses. Science, 295, 690-694.
66. Mesulam, M. M. (1998). From sensation to cognition. Brain, 121, 1013-1052.
67. Miller, R. (1991). Cortico-hippocampal interplay and the representation of contexts in the brain. Berlin: Springer-Verlag.
68. Mormann, F., Fell, J., Axmacher, N., Weber, B., Lehnertz, K., Elger, C. E., et al. (2005). Phase/amplitude reset and theta-gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus, 15, 890-900.
69. Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., & Rosenbaum, R. S. (2006). The cognitive neuroscience of remote episodic, semantic and spatial memory. Current Opinion in Neurobiology, 16, 179-190.
70. Nadel, L., & Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology, 7, 217-227.
71. Newman, J., & Grace, A. A. (1999). Binding across time: The selective gating of frontal and hippocampal systems modulating working memory and attentional states. Consciousness and Cognition, 8, 196-212.
72. Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapping, 15, 1-25.
73. Nir, Y., Fisch, L., Mukamel, R., Gelbard-Sagiv, H., Arieli, A., Fried, I., et al. (2007). Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Current Biology, 17, 1275-1285.
74. Osipova, D., Takashima, A., Oostenveld, R., Fernández, G., Maris, E., & Jensen, O. (2006). Theta and gamma oscillations predict encoding and retrieval of declarative memory. Journal of Neuroscience, 26, 7523-7531.
75. Palva, S., & Palva, J. M. (2007). New vistas for alpha-frequency band oscillations. Trends in Neurosciences, 304, 150-158.
76. Perrett, D. I., Rolls, E. T., & Caan, W. (1982). Visual neurones responsive to faces in the monkey temporal cortex. Experimental Brain Research, 47, 329-342.
77. Perrin, F., Pernier, J., Bertrand, O., & Echallier, J. F. (1989). Spherical splines for scalp potential and current density mapping. Electroencephalography and Clinical Neurophysiology, 72, 184-187.
78. Peskin, M., & Newell, F. N. (2004). Familiarity breeds attraction: Effects of exposure on the attractiveness of typical and distinctive faces. Perception, 33, 147-157.
79. Pexman, P. M., Hargreaves, I. S., Edwards, J. D., Henry, L. C., & Goodyear, B. G. (2007). The neural consequences of semantic richness: When more comes to mind, less activation is observed. Psychological Science, 18, 401-406.
80. Pfurtscheller, G. (2003). Induced oscillations in the alpha band: Functional meaning. Epilepsia, 44(Suppl. 12), 2-8.
81. Pulvermüller, F., Birbaumer, N., Lutzenberger, W., & Mohr, B. (1997). High-frequency brain activity: Its possible role in attention, perception and language processing. Progress in Neurobiology, 52, 427-445.
82. Ray, W. J., & Cole, H. W. (1985). EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. Science, 228, 750-752.
83. Röhm, D., Klimesch, W., Haider, H., & Doppelmayr, M. (2001). The role of theta and alpha oscillations for language comprehension in the human electroencephalogram. Neuroscience Letters, 310, 137-140.
84. Ryu, J. J., & Chaudhuri, A. (2007). Differences in attentional involvement underlying the perception of distinctive and typical faces. Perception, 36, 1057-1065.
85. Sauseng, P., Hoppe, J., Klimesch, W., Gerloff, C., & Hummel, F. C. (2007). Dissociation of sustained attention from central executive functions: Local activity and interregional connectivity in the theta range. European Journal of Neuroscience, 25, 587-593.
86. Sederberg, P. B., Gauthier, L. V., Terushkin, V., Miller, J. F., Barnathan, J. A., & Kahana, M. J. (2006). Oscillatory correlates of the primacy effect in episodic memory. Neuroimage, 32, 1422-1431.
87. 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.
88. Shah, A. S., Bressler, S. L., Knuth, K. H., Ding, M., Mehta, A. D., Ulbert, I., et al. (2004). Neural dynamics and fundamental mechanisms of event-related brain potentials. Cerebral Cortex, 14, 476-483.
89. Siapas, A. G., Lubenov, E. V., & Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron, 46, 141-151.
90. Singer, W., & Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annual Review of Neuroscience, 18, 555-586.
91. Steriade, M., Gloor, P., Llinás, R. R., Lopes de Silva, F. H., & Mesulam, M. M. (1990). Report of IFCN Committee on Basic Mechanisms. Basic mechanisms of cerebral rhythmic activities. Electroencephalography and Clinical Neurophysiology, 76, 481-508.
92. Tallon-Baudry, C., Bertrand, O., Delpuech, C., & Permier, J. (1996). Stimulus specificity of phase-locked and non-phase locked 40 Hz visual responses in human. Journal of Neuroscience, 16, 4240-4249.
93. Tallon-Baudry, C., Bertrand, O., Delpuech, C., & Permier, J. (1997). Oscillatory gamma-band 30-70 Hz. activity induced by a visual search task in humans. Journal of Neuroscience, 17, 722-734.
94. Tallon-Baudry, C., Bertrand, O., Hénaff, M. A., Isnard, J., & Fischer, C. (2005). Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cerebral Cortex, 15, 654-662.
95. Tanaka, J. W. (2001). The entry point of face recognition: Evidence for face expertise. Journal of Experimental Psychology: General, 130, 534-543.
96. Trautner, P., Rosburg, T., Dietl, T., Fell, J., Korzyukov, O. A., Kurthen, M., et al. (2006). Sensory gating of auditory evoked and induced gamma band activity in intracranial recordings. Neuroimage, 32, 790-798.
97. Treves, A., & Rolls, E. T. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus, 4, 374-391.
98. Tulving, E. (1983). Elements of episodic memory. New York: Oxford University Press.
99. Tulving, E. (1995). Organization of memory: Quo vadis? In M. S. Gazzaniga (Ed.), The cognitive neurosciences (pp. 839-847). Cambridge, MA: MIT Press.
100. Vogt, F., Klimesch, W., & Doppelmayr, M. (1998). High-frequency components in the alpha band and memory performance. Journal of Clinical Neurophysiology, 15, 167-172.
101. Von Stein, A., Chiang, C., & König, P. (2000). Top-down processing mediated by interareal synchronization. Proceedings of the National Academy of Sciences, U.S.A., 97, 14748-14753.
102. Weiss, S., & Rappelsberger, P. (2000). Long-range EEG synchronization during word encoding correlates with successful memory performance. Cognitive Brain Research, 9, 299-312.
103. Whitham, E. M., Lewis, T., Pope, K. J., Fitzgibbon, S. P., Clark, C. R., Loveless, S., et al. (2008). Thinking activates EMG in scalp electrical recordings. Clinical Neurophysiology, 119, 1166-1175.
104. Yovel, G., & Paller, K. A. (2004). The neural basis of the butcher-on-the-bus phenomenon: When a face seems familiar but is not remembered. Neuroimage, 21, 789-800.
105. Yuval-Greenberg, S., Tommer, O., Keren, A. S., Nelken, I., & Deuoell, L. Y. (2008). Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron, 58, 429-441.
106. Zion-Golumbic, E., & Bentin, S. (2007). Dissociated neural mechanisms for face detection and configural encoding: Evidence from N170 and induced gamma-band oscillation effects. Cerebral Cortex, 17, 1741-1749.
107. Zion-Golumbic, E., Golan, T., Anaki, D., & Bentin, S. (2008). Human face preference in gamma-frequency EEG activity. Neuroimage, 39, 1980-1987.