Transverse patterning dissociates human EEG theta power and hippocampal BOLD activation

Psychophysiology

Volumn 46, Issue 1, 2009, Pages 153-162

  Meltzer, Jed A ^a,d   Fonzo, Greg A ^a   Constable, R Todd ^a,b,c  

^a YALE UNIVERSITY   (United States)

^b Yale University   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

Alpha; Default mode; fMRI; LORETA; Negative BOLD

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; BLOOD OXYGENATION; BLOOD OXYGENATION LEVEL DEPENDENT; ELECTROENCEPHALOGRAM; ELECTROMAGNETIC FIELD; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; HUMAN; HUMAN EXPERIMENT; MEMORY; MODULATION; NORMAL HUMAN; OSCILLATION; PARIETAL LOBE; PRIORITY JOURNAL; TASK PERFORMANCE; THETA RHYTHM; TOPOGRAPHY;

EID: 58149133602     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/j.1469-8986.2008.00719.x     Document Type: Article

References (90)

1. Alvarado, M. C. Rudy, J. W. (1995). Rats with damage to the hippocampal-formation are impaired on the transverse-patterning problem but not on elemental discriminations. Behavioral Neuroscience, 109, 204 211.
2. Alvarado, M. C., Wright, A. A. Bachevalier, J. (2002). Object and spatial relational memory in adult rhesus monkeys is impaired by neonatal lesions of the hippocampal formation but not the amygdaloid complex. Hippocampus, 12, 421 433.
3. Asada, H., Fukuda, Y., Tsunoda, S., Yamaguchi, M. Tonoike, M. (1999). Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulate cortex in humans. Neuroscience Letters, 274, 29 32.
4. Astur, R. S. Constable, R. T. (2004). Hippocampal dampening during a relational memory task. Behavioral Neuroscience, 118, 667 675.
5. Astur, R. S. Sutherland, R. J. (1998). Relational learning in humans: The transverse patterning problem. Psychobiology, 26, 176 182.
6. Axmacher, N., Mormann, F., Fernandez, G., Elger, C. E. Fell, J. (2006). Memory formation by neuronal synchronization. Brain Research. Brain Research Reviews, 52, 170 182.
7. Bastiaansen, M. Hagoort, P. (2003). Event-induced theta responses as a window on the dynamics of memory. Cortex, 39, 967 992.
8. Bastiaansen, M. C., van Berkum, J. J. Hagoort, P. (2002). Event-related theta power increases in the human EEG during online sentence processing. Neuroscience Letters, 323, 13 16.
9. Bland, B. H. Oddie, S. D. (2001). Theta band oscillation and synchrony in the hippocampal formation and associated structures: The case for its role in sensorimotor integration. Behavioural Brain Research, 127, 119 136.
10. Borisyuk, R. M. Hoppensteadt, F. C. (1998). Memorizing and recalling spatial-temporal patterns in an oscillator model of the hippocampus. Biosystems, 48, 3 10.
11. Brookes, M. J., Gibson, A. M., Hall, S. D., Furlong, P. L., Barnes, G. R., Hillebrand, A., et al 2005). GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS co-localisation with fMRI BOLD response in visual cortex. NeuroImage, 26, 302 308.
12. 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.
13. Bussey, T. J., Clea Warburton, E., Aggleton, J. P. Muir, J. L. (1998). Fornix lesions can facilitate acquisition of the transverse patterning task: A challenge for "configural" theories of hippocampal function. Journal of Neuroscience, 18, 1622 1631.
14. Buzsaki, G. (1996). The hippocampo-neocortical dialogue. Cerebral Cortex, 6, 81 92.
15. Caplan, J. B. Glaholt, M. G. (2007). The roles of EEG oscillations in learning relational information. NeuroImage, 15, 15.
16. Caplan, J. B., Madsen, J. R., Raghavachari, S. Kahana, M. J. (2001). Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. Journal of Neurophysiology, 86, 368 380.
17. Ciulla, C., Takeda, T. Endo, H. (1999). MEG characterization of spontaneous alpha rhythm in the human brain. Brain Topography, 11, 211 222.
18. de Araujo, D. B., Baffa, O. Wakai, R. T. (2002). Theta oscillations and human navigation: A magnetoencephalography study. Journal of Cognitive Neuroscience, 14, 70 78.
19. Delorme, A. Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134, 9 21.
20. Dusek, J. A. Eichenbaum, H. (1998). The hippocampus and transverse patterning guided by olfactory cues. Behavioral Neuroscience, 112, 762 771.
21. Ekstrom, A., Viskontas, I., Kahana, M., Jacobs, J., Upchurch, K., Bookheimer, S., et al 2007). Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus, 17, 606 617.
22. Ekstrom, A. D., Caplan, J. B., Ho, E., Shattuck, K., Fried, I. Kahana, M. J. (2005). Human hippocampal theta activity during virtual navigation. Hippocampus, 15, 881 889.
23. Fell, J., Klaver, P., Elfadil, H., Schaller, C., Elger, C. E. Fernandez, G. (2003). Rhinal-hippocampal theta coherence during declarative memory formation: Interaction with gamma synchronization? European Journal of Neuroscience, 17, 1082 1088.
24. Foucher, J. R., Otzenberger, H. Gounot, D. (2003). The BOLD response and the gamma oscillations respond differently than evoked potentials: An interleaved EEG-fMRI study. BMC Neuroscience, 4, 22.
25. Frei, E., Gamma, A., Pascual-Marqui, R., Lehmann, D., Hell, D. Vollenweider, F. X. (2001). Localization of MDMA-induced brain activity in healthy volunteers using low resolution brain electromagnetic tomography (LORETA). Human Brain Mapping, 14, 152 165.
26. Gabrieli, J. D., Brewer, J. B., Desmond, J. E. Glover, G. H. (1997). Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science, 276, 264 266.
27. Goldman, R. I., Stern, J. M., Engel, J., Jr. Cohen, M. S. (2002). Simultaneous EEG and fMRI of the alpha rhythm. NeuroReport, 13, 2487 2492.
28. Goncalves, S. I., de Munck, J. C., Pouwels, P. J., Schoonhoven, R., Kuijer, J. P., Maurits, N. M., et al 2006). Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability. NeuroImage, 30, 203 213.
29. Guderian, S. Duzel, E. (2005). Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus, 15, 901 912.
30. Gusnard, D. A. Raichle, M. E. (2001). Searching for a baseline: Functional imaging and the resting human brain. Nature Reviews. Neuroscience, 2, 685 694.
31. Hasselmo, M. E. (2005). What is the function of hippocampal theta rhythm? Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus, 15, 936 949.
32. Hasselmo, M. E., Hay, J., Ilyn, M. Gorchetchnikov, A. (2002). Neuromodulation, theta rhythm and rat spatial navigation. Neural Networks, 15, 689 707.
33. Hyman, J. M., Zilli, E. A., Paley, A. M. Hasselmo, M. E. (2005). Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus, 15, 739 749.
34. Ishii, R., Shinosaki, K., Ukai, S., Inouye, T., Ishihara, T., Yoshimine, T., et al 1999). Medial prefrontal cortex generates frontal midline theta rhythm. NeuroReport, 10, 675 679.
35. Jensen, O. Lisman, J. E. (2005). Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends in Neurosciences, 28, 67 72.
36. Jensen, O. Tesche, C. D. (2002). Frontal theta activity in humans increases with memory load in a working memory task. European Journal of Neuroscience, 15, 1395 1399.
37. Jones, M. W. Wilson, M. A. (2005). Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biology, 3, e402.
38. Kahana, M. J., Seelig, D. Madsen, J. R. (2001). Theta returns. Current Opinion in Neurobiology, 11, 739 744.
39. Kilner, J. M., Mattout, J., Henson, R. Friston, K. J. (2005). Hemodynamic correlates of EEG: A heuristic. Neuroimage, 28, 280 286.
40. Klimesch, W., Doppelmayr, M., Russegger, H. Pachinger, T. (1996). Theta band power in the human scalp EEG and the encoding of new information. NeuroReport, 7, 1235 1240.
41. Klimesch, W., Doppelmayr, M., Schwaiger, J., Auinger, P. Winkler, T. (1999). 'Paradoxical' alpha synchronization in a memory task. Brain Research. Cognitive Brain Research, 7, 493 501.
42. 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, 1, 1.
43. Laufs, H., Holt, J. L., Elfont, R., Krams, M., Paul, J. S., Krakow, K., et al 2006). Where the BOLD signal goes when alpha EEG leaves. NeuroImage, 31, 1408 1418.
44. Laufs, H., Kleinschmidt, A., Beyerle, A., Eger, E., Salek-Haddadi, A., Preibisch, C., et al 2003). EEG-correlated fMRI of human alpha activity. NeuroImage, 19, 1463 1476.
45. Lee, H., Simpson, G. V., Logothetis, N. K. Rainer, G. (2005). Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron, 45, 147 156.
46. Lisman, J. (2005). The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus, 15, 913 922.
47. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T. Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150 157.
48. Luu, P., Tucker, D. M. Makeig, S. (2004). Frontal midline theta and the error-related negativity: Neurophysiological mechanisms of action regulation. Clinical Neurophysiology, 115, 1821 1835.
49. Makeig, S. (1993). Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalography and Clinical Neurophysiology, 86, 283 293.
50. Martinez-Montes, E., Valdes-Sosa, P. A., Miwakeichi, F., Goldman, R. I. Cohen, M. S. (2004). Concurrent EEG/fMRI analysis by multiway Partial Least Squares. NeuroImage, 22, 1023 1034.
51. McKiernan, K. A., Kaufman, J. N., Kucera-Thompson, J. Binder, J. R. (2003). A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience, 15, 394 408.
52. Meltzer, J. A. Constable, R. T. (2005). Activation of human hippocampal formation reflects success in both encoding and cued recall of paired associates. NeuroImage, 24, 384 397.
53. Meltzer, J. A., Negishi, M. Constable, R. T. (2008). Biphasic hemodynamic responses influence deactivation and may mask activation in block-design fMRI paradigms. Human Brain Mapping, 29, 385 399.
54. Meltzer, J. A., Negishi, M., Mayes, L. C. Constable, R. T. (2007). Individual differences in EEG theta and alpha dynamics during working memory correlate with fMRI responses across subjects. Clinical Neurophysiology, 118, 2419 2436.
55. Meltzer, J. A., Zaveri, H. P., Goncharova, I. I., Distasio, M. M., Papademetris, X., Spencer, S. S., et al 2008). Effects of working memory load on oscillatory power in human intracranial EEG. Cerebral Cortex, 18, 1843 1855.
56. Michel, C. M., Murray, M. M., Lantz, G., Gonzalez, S., Spinelli, L. Grave de Peralta, R. (2004). EEG source imaging. Clinical Neurophysiology, 115, 2195 2222.
57. Miller, R. (1991). Cortico-hippocampal interplay and the representation of contexts in the brain. Heidelberg : Springer-Verlag.
58. Mizuhara, H., Wang, L. Q., Kobayashi, K. Yamaguchi, Y. (2004). A long-range cortical network emerging with theta oscillation in a mental task. NeuroReport, 15, 1233 1238.
59. Moore, R. A., Gale, A., Morris, P. H. Forrester, D. (2006). Theta phase locking across the neocortex reflects cortico-hippocampal recursive communication during goal conflict resolution. International Journal of Psychophysiology, 60, 260 273.
60. Moosmann, M., Ritter, P., Krastel, I., Brink, A., Thees, S., Blankenburg, F., et al 2003). Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. NeuroImage, 20, 145 158.
61. Mukamel, R., Gelbard, H., Arieli, A., Hasson, U., Fried, I. Malach, R. (2005). Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science, 309, 951 954.
62. Niessing, J., Ebisch, B., Schmidt, K. E., Niessing, M., Singer, W. Galuske, R. A. (2005). Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science, 309, 948 951.
63. Nunez, P. L. Srinivasan, R. (2006). Electric fields of the brain: The neurophysics of EEG. Oxford : Oxford University Press.
64. O'Keefe, J. Recce, M. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus, 3, 317 330.
65. Onton, J., Delorme, A. Makeig, S. (2005). Frontal midline EEG dynamics during working memory. NeuroImage, 27, 341 356.
66. Otten, L. J., Henson, R. N. Rugg, M. D. (2001). Depth of processing effects on neural correlates of memory encoding: Relationship between findings from across- and within-task comparisons. Brain, 124, 399 412.
67. Pascual-Marqui, R. D., Michel, C. M. Lehmann, D. (1994). Low resolution electromagnetic tomography: A new method for localizing electrical activity in the brain. International Journal of Psychophysiology, 18, 49 65.
68. Percival, D. B. Walden, A. T. (1993). Spectral analysis for physical applications. Cambridge : Cambridge University Press.
69. Raghavachari, S., Kahana, M. J., Rizzuto, D. S., Caplan, J. B., Kirschen, M. P., Bourgeois, B., et al 2001). Gating of human theta oscillations by a working memory task. Journal of Neuroscience, 21, 3175 3183.
70. Raghavachari, S., Lisman, J. E., Tully, M., Madsen, J. R., Bromfield, E. B. Kahana, M. J. (2006). Theta oscillations in human cortex during a working-memory task: Evidence for local generators. Journal of Neurophysiology, 95, 1630 1638.
71. Reber, P. J., Siwiec, R. M., Gitelman, D. R., Parrish, T. B., Mesulam, M. M., Paller, K. A., et al 2002). Neural correlates of successful encoding identified using functional magnetic resonance imaging. Journal of Neuroscience, 22, 9541 9548.
72. Reed, J. M. Squire, L. R. (1999). Impaired transverse patterning in human amnesia is a special case of impaired memory for two-choice discrimination tasks. Behavioral Neuroscience, 113, 3 9.
73. Rickard, T. C. Grafman, J. (1998). Losing their configural mind. Amnesic patients fail on transverse patterning. Journal of Cognitive Neuroscience, 10, 509 524.
74. Rickard, T. C., Verfaellie, M. Grafman, J. (2006). Transverse patterning and human amnesia. Journal of Cognitive Neuroscience, 18, 1723 1733.
75. Sammer, G., Blecker, C., Gebhardt, H., Bischoff, M., Stark, R., Morgen, K., et al 2007). Relationship between regional hemodynamic activity and simultaneously recorded EEG-theta associated with mental arithmetic-induced workload. Human Brain Mapping, 28, 793 803.
76. Sanchez-Arroyos, R., Gaztelu, J. M., Zaplana, J., Dajas, F. Garcia-Austt, E. (1993). Hippocampal and entorhinal glucose metabolism in relation to cholinergic theta rhythm. Brain Research Bulletin, 32, 171 178.
77. Scheeringa, R., Bastiaansen, M. C., Petersson, K. M., Oostenveld, R., Norris, D. G. Hagoort, P. (2007). Frontal theta EEG activity correlates negatively with the default mode network in resting state. International Journal of Psychophysiology, 67, 242 251.
78. 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.
79. Shulman, G. L., Fiez, J. A., Corbetta, M., Buckner, R. L., Miezin, F. M., Raichle, M. E., et al 1997). Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. Journal of Cognitive Neuroscience, 9, 648 663.
80. Siapas, A. G., Lubenov, E. V. Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron, 46, 141 151.
81. Spence, K. W. (1952). The nature of response in discrimination learning. Psychology Review, 59, 89 93.
82. Stark, C. E. Squire, L. R. (2000). Functional magnetic resonance imaging (fMRI) activity in the hippocampal region during recognition memory. Journal of Neuroscience, 20, 7776 7781.
83. Tsujimoto, T., Shimazu, H. Isomura, Y. (2006). Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. Journal of Neurophysiology, 95, 2987 3000.
84. Tuladhar, A. M., Huurne, N. T., Schoffelen, J. M., Maris, E., Oostenveld, R. Jensen, O. (2007). Parieto-occipital sources account for the increase in alpha activity with working memory load. Human Brain Mapping, 31, 31.
85. Uchida, S., Maehara, T., Hirai, N., Kawai, K. Shimizu, H. (2003). Theta oscillation in the anterior cingulate and beta-1 oscillation in the medial temporal cortices: A human case report. Journal of Clinical Neuroscience, 10, 371 374.
86. Uecker, A., Barnes, C. A., McNaughton, B. L. Reiman, E. M. (1997). Hippocampal glycogen metabolism, EEG, and behavior. Behavioral Neuroscience, 111, 283 291.
87. Vanni, S., Revonsuo, A. Hari, R. (1997). Modulation of the parieto-occipital alpha rhythm during object detection. Journal of Neuroscience, 17, 7141 7147.
88. Wang, C., Ulbert, I., Schomer, D. L., Marinkovic, K. Halgren, E. (2005). Responses of human anterior cingulate cortex microdomains to error detection, conflict monitoring, stimulus-response mapping, familiarity, and orienting. Journal of Neuroscience, 25, 604 613.
89. Yamagishi, N., Callan, D. E., Goda, N., Anderson, S. J., Yoshida, Y. Kawato, M. (2003). Attentional modulation of oscillatory activity in human visual cortex. NeuroImage, 20, 98 113.
90. Yamaguchi, Y., Aota, Y., Sato, N., Wagatsuma, H. Wu, Z. (2004). Synchronization of neural oscillations as a possible mechanism underlying episodic memory: A study of theta rhythm in the hippocampus. Journal of Integrative Neuroscience, 3, 143 157.