Selective theta-synchronization of choice-relevant information subserves goal-directed behavior

Frontiers in Human Neuroscience

Volumn 4, Issue , 2010, Pages

  Womelsdorf, Thilo ^a   Vinck, Martin ^b   Stan Leung, L ^a   Everling, Stefan ^a,c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Cognitive control; Decision making; Oscillation; Reinforcement learning; Theta synchronization

Indexed keywords

ANTICIPATION; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CINGULATE GYRUS; DECISION MAKING; EVIDENCE BASED PRACTICE; HIPPOCAMPUS THETA RHYTHM; HUMAN; LIMBIC CORTEX; NERVE MEMBRANE; NONHUMAN; OSCILLATION; STIMULUS RESPONSE; STRIATE CORTEX; TASK PERFORMANCE; THETA RHYTHM; WORKING MEMORY;

EID: 79953014574     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2010.00210     Document Type: Article

References (153)

1. Adhikari, A., Topiwala, M. A., and Gordon, J. A. (2010). Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65, 257-269.
2. Aggleton, J. P., Shaw, C., and Gaffan, E. A. (1992). The performance of postencephalitic amnesic subjects on two behavioural tests of memory: concurrentdiscrimination learning and delayed matching-to-sample. Cortex 28, 359-372.
3. Alonso, A., and Llinas, R. R. (1989). Subthreshold Na+-dependent thetalike rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342, 175-177.
4. Asada, H., Fukuda, Y., Tsunoda, S., Yamaguchi, M., and Tonoike, M. (1999). Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulated cortex in humans. Neurosci. Lett. 274, 29-32.
5. Axmacher, N., Henseler, M. M., Jensen, O., Weinreich, I., Elger, C. E., and Fell, J. (2010). Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc. Natl. Acad. Sci. U.S.A. 107, 3228-3233.
6. Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P., Gioanni, Y., Battaglia, F. P., and Wiener, S. I. (2010). Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66, 921-936.
7. Berke, J. D. (2009). Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur. J. Neurosci. 30, 848-859.
8. Bilkey, D. K., and Heinemann, U. (1999). Intrinsic theta-frequency membrane potential oscillations in layer III/V perirhinal cortex neurons of the rat. Hippocampus 9, 510-518.
9. Bland, B. H., and Colom, L. V. (1993). Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog. Neurobiol. 41, 157-208.
10. Bontempi, B., Laurent-Demir, C., Destrade, C., and Jaffard, R. (1999). Time-dependent reorganization of brain circuitry underlying longterm memory storage. Nature 400, 671-675.
11. Borst, J. G., Leung, L. W., and MacFabe, D. F. (1987). Electrical activity of the cingulate cortex. II. Cholinergic modulation. Brain Res. 407, 81-93.
12. Burwell, R. D., and Witter, M. P. (2002). Basic anatomy of the parahippocampalregion in monkeys and rats, in The Parahippocampal Region, eds M. P. Witter and F. G. Wouterlood (New York: Oxford University Press), 53-59.
13. Buschman, T. J., and Miller, E. K. (2009). Serial, covert shifts of attention during visual search are reflected by the frontal eye fields and correlated withpopulation oscillations. Neuron 63, 386-396.
14. Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340.
15. Buzsaki, G. (2006). Rhythms of the Brain. Oxford, NY: Oxford University Press Inc.
16. Cantero, J. L., Atienza, M., Stickgold, R., Kahana, M. J., Madsen, J. R., and Kocsis, B. (2003). Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23, 10897-10903.
17. Cardin, J. A., Carlen, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L. H., and Moore, C. I. (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667.
18. Cashdollar, N., Malecki, U., Rugg-Gunn, F. J., Duncan, J. S., Lavie, N., and Duzel, E. (2009). Hippocampus-dependent and -independent theta-networks of active maintenance. Proc. Natl. Acad. Sci. U.S.A. 106, 20493-20498.
19. Chapman, C. A., and Lacaille, J. C. (1999a). Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneuronsand pacing of pyramidal cell firing. J. Neurosci. 19, 8637-8645.
20. Chapman, C. A., and Lacaille, J. C. (1999b). Intrinsic theta-frequencymembrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J. Neurophysiol. 81, 1296-1307.
21. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., and Somogyi, P. (1995). Synchronization of neuronal activityin hippocampus by individual GABAergic interneurons. Nature 378, 75-78.
22. Colgin, L. L., Denninger, T., Fyhn, M., Hafting, T., Bonnevie, T., Jensen, O., Moser, M. B., and Moser, E. I. (2009). Frequency of gamma oscillationsroutes flow of information in the hippocampus. Nature 462, 353-357.
23. Collins, D. R., Lang, E. J., and Pare, D. (1999). Spontaneous activity of the perirhinal cortex in behaving cats. Neuroscience 89, 1025-1039.
24. Debener, S., Ullsperger, M., Siegel, M., Fiehler, K., von Cramon, D. Y., and Engel, A. K. (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J. Neurosci. 25, 11730-11737.
25. DeCoteau, W. E., Thorn, C., Gibson, D. J., Courtemanche, R., Mitra, P., Kubota, Y., and Graybiel, A. M. (2007a). Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J. Neurophysiol. 97, 3800-3805.
26. DeCoteau, W. E., Thorn, C., Gibson, D. J., Courtemanche, R., Mitra, P., Kubota, Y., and Graybiel, A. M. (2007b). Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc. Natl. Acad. Sci. U.S.A. 104, 5644-5649.
27. Dehaene, S., and Changeux, J. P. (2000). Reward-dependent learning in neuronalnetworks for planning and decision making. Prog. Brain Res. 126, 217-229.
28. Douglas, R. J., and Martin, K. A. (2007). Mapping the matrix: the ways of neocortex. Neuron 56, 226-238.
29. Duzel, E., Penny, W. D., and Burgess, N. (2010). Brain oscillations and memory. Curr. Opin. Neurobiol. 20, 143-149.
30. Feenstra, B. W., and Holsheimer, J. (1979). Dipole-like neuronal sources of thetarhythm in dorsal hippocampus, dentate gyrus and cingulate cortex of the urethane-anesthetized rat. Electroencephalogr. Clin. Neurophysiol. 47, 532-538.
31. Fell, J., Klaver, P., Elfadil, H., Schaller, C., Elger, C. E., and Fernandez, G. (2003). Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? Eur. J. Neurosci. 17, 1082-1088.
32. Fell, J., Klaver, P., Lehnertz, K., Grunwald, T., Schaller, C., Elger, C. E., and Fernandez, G. (2001). Human memory formation is accompanied by rhinal- hippocampal coupling and decoupling. Nat. Neurosci. 4, 1259-1264.
33. Frankland, P. W., Bontempi, B., Talton, L. E., Kaczmarek, L., and Silva, A. J. (2004). The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304, 881-883.
34. Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu.Rev. Neurosci. 32, 209-224.
35. Gevins, A., Smith, M. E., McEvoy, L., and Yu, D. (1997). High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb. Cortex 7, 374-385.
36. Glimcher, P. W., Camerer, C. F., Fehr, E., and Poldrack, R. A. (2009). Introduction: a brief history of neuroeconomics, in Neuroeconomics: Decision Making and the Brain, eds P. W. Glimcher, C. F. Camerer, E. Fehr, and R. A. Poldrack (London: Academic Press), 1-13.
37. Gold, J. I., and Shadlen, M. N. (2007). The neural basis of decision making. Annu. Rev. Neurosci. 30, 535-574.
38. Goutagny, R., Jackson, J., and Williams, S. (2009). Self-generated theta oscillations in the hippocampus. Nat. Neurosci. 12, 1491-1493.
39. Guderian, S., and Duzel, E. (2005). Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus 15, 901-912.
40. Guderian, S., Schott, B. H., Richardson-Klavehn, A., and Duzel, E. (2009). Medial temporal theta state before an event predicts episodic encodingsuccess in humans. Proc. Natl. Acad. Sci. U.S.A. 106, 5365-5370.
41. Gutfreund, Y., Yarom, Y., and Segev, I. (1995). Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modelling. J. Physiol. 483(Pt 3), 621-640.
42. Haber, S. N., and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4-26.
43. Hannula, D. E., Tranel, D., and Cohen, N. J. (2006). The long and the short of it: relational memory impairments in amnesia, even at short lags. J. Neurosci. 26, 8352-8359.
44. Harvey, C. D., Collman, F., Dombeck, D. A., and Tank, D. W. (2009). Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946.
45. Hassabis, D., Kumaran, D., Vann, S. D., and Maguire, E. A. (2007). Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl. Acad. Sci. U.S.A. 104, 1726-1731.
46. 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.
47. Hu, H., Vervaeke, K., and Storm, J. F. (2002). Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J. Physiol. 545, 783-805.
48. Hutcheon, B., and Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222.
49. Huxter, J. R., Senior, T. J., Allen, K., and Csicsvari, J. (2008). Theta phasespecific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587-594.
50. Hyman, J. M., Zilli, E. A., Paley, A. M., and Hasselmo, M. E. (2005). Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 15, 739-749.
51. Hyman, j. M., Zilli, E. A., Paley, A. M., and Hasselmo, M. E. (2010). Working memory performance correlates with prefrontal-hippocampal theta interactionsbut not with prefrontal neuron firing rates. Front. Integr. Neurosci. 4:2. doi: 10.3389/neuro.07.002.2010.
52. Ishii, R., Shinosaki, K., Ukai, S., Inouye, T., Ishihara, T., Yoshimine, T., Hirabuki, N., Asada, H., Kihara, T., Robinson, S. E., and Takeda, M. (1999). Medial prefrontal cortex generates frontal midline theta rhythm. Neuroreport 10, 675-679.
53. Itskov, V., Pastalkova, E., Mizuseki, K., Buzsaki, G., and Harris, K. D. (2008). Theta-mediated dynamics of spatial information in hippocampus. J. Neurosci. 28, 5959-5964.
54. Jacobs, J., Hwang, G., Curran, T., and Kahana, M. J. (2006). EEG oscillations and recognition memory: theta correlates of memory retrieval and decision making. Neuroimage 32, 978-987.
55. Jensen, O., and Lisman, J. E. (1998). An oscillatory short-term memory buffer model can account for data on the Sternberg task. J. Neurosci. 18, 10688-10699.
56. Jensen, O., and Lisman, J. E. (2000). Position reconstruction from anensemble of hippocampal place cells: contribution of theta phase coding. J. Neurophysiol. 83, 2602-2609.
57. Jensen, O., and Tesche, C. D. (2002). Frontal theta activity in humansincreases with memory load in a working memory task. Eur. J. Neurosci. 15, 1395-1399.
58. Johnson, A., and Redish, A. D. (2007). Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176-12189.
59. Johnson, A., van der Meer, M. A., and Redish, A. D. (2007). Integrating hippocampusand striatum in decisionmaking. Curr. Opin. Neurobiol. 17, 692-697.
60. Johnston, K., Levin, H. M., Koval, M. J., and Everling, S. (2007). Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neuronsfollowing task switching. Neuron 53, 453-462.
61. Jones, M. W., and Wilson, M. A. (2005a). Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3, e402. doi: 10.1371/journal.pbio.0030402.
62. Jones, M. W., and Wilson, M. A. (2005b). Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15, 867-873.
63. Kahana, M. J. (2006). The cognitive correlates of human brain oscillations. J. Neurosci. 26, 1669-1672.
64. Kamondi, A., Acsady, L., Wang, X. J., and Buzsaki, G. (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activitydependent phase-precession of action potentials. Hippocampus 8, 244-261.
65. Kayser, C., Montemurro, M. A., Logothetis, N. K., and Panzeri, S. (2009). Spikephase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61, 597-608.
66. Kennerley, S. W., Walton, M. E., Behrens, T. E., Buckley, M. J., and Rushworth, M. F. (2006). Optimal decision makingand the anterior cingulate cortex. Nat. Neurosci. 9, 940-947.
67. Kerns, J. G., Cohen, J. D., MacDonald, A. W. III, Cho, R. Y., Stenger, V. A., and Carter, C. S. (2004). Anterior cingulated conflict monitoring and adjustments in control. Science 303, 1023-1026.
68. Kimchi, E. Y., Torregrossa, M. M., Taylor, J. R., and Laubach, M. (2009). Neuronal correlates of instrumental learning in the dorsal striatum. J. Neurophysiol. 102, 475-489.
69. Kirk, I. J., Oddie, S. D., Konopacki, J., and Bland, B. H. (1996). Evidence for differential control of posterior hypothalamic, supramammillary, and medialmammillary theta-related cellular discharge by ascending and descending pathways. J. Neurosci. 16, 5547-5554.
70. Klausberger, T., Magill, P. J., Marton, L. F., Roberts, J. D., Cobden, P. M., Buzsaki, G., and Somogyi, P. (2003). Brainstate- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848.
71. Klausberger, T., and Somogyi, P. (2008). Neuronal diversity and temporaldynamics: the unity of hippocampal circuit operations. Science 321, 53-57.
72. Kocsis, B., Di Prisco, G. V., and Vertes, R. P. (2001). Theta synchronization in the limbic system: the role of Gudden'stegmental nuclei. Eur. J. Neurosci. 13, 381-388.
73. Krause, C. M., Sillanmaki, L., Koivisto, M., Saarela, C., Haggqvist, A., Laine, M., and Hamalainen, H. (2000). The effects of memory load on eventrelated EEG desynchronization and synchronization. Clin. Neurophysiol. 111, 2071-2078.
74. Lansink, C. S., Goltstein, P. M., Lankelma, J. V., McNaughton, B. L., and Pennartz, C. M. (2009). Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 7, e1000173. doi: 10.1371/journal.pbio.1000173.
75. Lee, H., Simpson, G. V., Logothetis, N. K., and Rainer, G. (2005). Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45, 147-156.
76. Leung, L. S. (1998). Generation of theta and gamma rhythms in the hippocampus. Neurosci. Biobehav. Rev. 22, 275-290.
77. Leung, L. S., and Yim, C. Y. (1986). Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res. 367, 323-327.
78. Leung, L. S., and Yu, H. W. (1998). Thetafrequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J.Neurophysiol. 79, 1592-1596.
79. Lisman, J., and Buzsaki, G. (2008). A neural coding scheme formed by thecombined function of gamma and theta oscillations. Schizophr. Bull. 34, 974-980.
80. Lisman, J. E., and Idiart, M. A. (1995). Storage of 7+/-2 short-term memories in oscillatory subcycles. Science267, 1512-1515.
81. Luu, P., Tucker, D. M., and Makeig, S. (2004). Frontal midline theta andthe error-related negativity: neurophysiological mechanisms of actionregulation. Clin Neurophysiol 115,1821-1835.
82. Mansouri, F. A., Tanaka, K., and Buckley, M. J. (2009). Conflict-induced behaviouraladjustment: a clue to the executive functions of the prefrontal cortex. Nat. Rev. Neurosci. 10, 141-152.
83. McEvoy, L. K., Pellouchoud, E., Smith, M. E., and Gevins, A. (2001). Neurophysiological signals of working memory in normal aging. Brain Res. Cogn. Brain Res. 11, 363-376.
84. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., and Moser, M. B. (2006a). Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678.
85. McNaughton, N., Ruan, M., and Woodnorth, M. A. (2006b). Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16, 1102-1110.
86. McNaughton, N., Logan, B., Panickar, K. S., Kirk, I. J., Pan, W. X., Brown, N. T., and Heenan, A. (1995). Contribution of synapses in the medial supramammillarynucleus to the frequency of hippocampal theta rhythm in freely moving rats. Hippocampus 5, 534-545.
87. Meltzer, J. A., Zaveri, H. P., Goncharova, I. I., Distasio, M. M., Papademetris, X., Spencer, S. S., Spencer, D. D., and Constable, R. T. (2008). Effects of working memory load on oscillatory power in human intracranial EEG. Cereb. Cortex 18, 1843-1855.
88. Michels, L., Moazami-Goudarzi, M., Jeanmonod, D., and Sarnthein, J. (2008). EEG alpha distinguishes between cuneal and precuneal activation in working memory. Neuroimage 40, 1296-1310.
89. Miller, E. K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59-65.
90. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202.
91. Mizuhara, H., and Yamaguchi, Y. (2007). Human cortical circuits for centralexecutive function emerge by theta phase synchronization. Neuroimage 36, 232-244.
92. Mizuhara, H., Wang, L. Q., Kobayashi, K., and Yamaguchi, Y. (2004). A longrange cortical network emerging withtheta oscillation in a mental task. Neuroreport 15, 1233-1238.
93. Mizuseki, K., Sirota, A., Pastalkova, E., and Buzsaki, G. (2009). Theta oscillations provide temporal windows for local circuit computation in theentorhinal-hippocampal loop. Neuron 64, 267-280.
94. Mormann, F., Fell, J., Axmacher, N., Weber, B., Lehnertz, K., Elger, C. E., and Fernandez, G. (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.
95. Mormann, F., Kornblith, S., Quiroga, R. Q., Kraskov, A., Cerf, M., Fried, I., and Koch, C. (2008a). Latency and selectivity of single neurons indicatehierarchical processing in the human medial temporal lobe. J. Neurosci. 28,8865-8872.
96. Mormann, F., Osterhage, H., Andrzejak, R. G., Weber, B., Fernandez, G., Fell, J., Elger, C. E., and Lehnertz, K. (2008b). Independent delta/theta rhythms inthe human hippocampus and entorhinal cortex. Front. Hum. Neurosci. 2:3. doi: 10.3389/neuro.09.003.2008.
97. O'Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., and Dolan, R. J. (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452-454.
98. Olson, I. R., Page, K., Moore, K. S., Chatterjee, A., and Verfaellie, M.(2006). Working memory for conjunctions relies on the medial temporal lobe. J. Neurosci. 26, 4596-4601.
99. Onton, J., Delorme, A., and Makeig, S. (2005). Frontal midline EEG dynamics during working memory. Neuroimage 27, 341-356.
100. Padoa-Schioppa, C., and Assad, J. A. (2006). Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223-226.
101. Panzeri, S., Brunel, N., Logothetis, N. K., and Kayser, C. (2010). Sensory neuralcodes using multiplexed temporal scales. Trends Neurosci. 33, 111-120.
102. Pastalkova, E., Itskov, V., Amarasingham, A., and Buzsaki, G. (2008). Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322-1327.
103. Payne, L., and Kounios, J. (2009). Coherent oscillatory networks supporting shortterm memory retention. Brain Res. 1247, 126-132.
104. Paz, R., Bauer, E. P., and Pare, D. (2008). Theta synchronizes the activity of medial prefrontal neurons during learning. Learn. Mem. 15, 524-531.
105. Pedemonte, M., Pena, J. L., and Velluti, R. A. (1996). Firing of inferior colliculusauditory neurons is phase-locked to the hippocampus theta rhythm duringparadoxical sleep and waking. Exp. Brain Res. 112, 41-46.
106. Pennartz, C. M., Berke, J. D., Graybiel, A. M., Ito, R., Lansink, C. S., van der Meer, M., Redish, A. D., Smith, K. S., and Voorn, P. (2009). Corticostriatal interactions during learning, memory processing, and decision making. J. Neurosci. 29, 12831-12838.
107. Petsche, H., Stumpf, C., and Gogolak, G. (1962). The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroencephalogr. Clin. Neurophysiol. 14, 202-211.
108. Popescu, A. T., Popa, D., and Pare, D.(2009). Coherent gamma oscillations couple the amygdala and striatum during learning. Nat. Neurosci. 12, 801-807.
109. Raghavachari, S., Kahana, M. J., Rizzuto, D. S., Caplan, J. B., Kirschen, M. P., Bourgeois, B., Madsen, J. R., and Lisman, J. E. (2001). Gating of humantheta oscillations by a working memorytask. J. Neurosci. 21, 3175-3183.
110. Raghavachari, S., Lisman, J. E., Tully, M., Madsen, J. R., Bromfield, E. B., and Kahana, M. J. (2006). Theta oscillations in human cortex during a working-memory task: evidence for local generators. J. Neurophysiol. 95, 1630-1638.
111. Ramus, S. J., Davis, J. B., Donahue, R. J., Discenza, C. B., and Waite, A. A. (2007). Interactions between the orbitofrontal cortex and the hippocampal memory system during the storage of long-term memory. Ann. N. Y. Acad. Sci. 1121, 216-231.
112. Rizzuto, D. S., Madsen, J. R., Bromfield, E. B., Schulze-Bonhage, A., Seelig, D., Aschenbrenner-Scheibe, R., and Kahana, M. J. (2003). Reset of human neocortical oscillations during a working memory task. Proc. Natl. Acad. Sci. U.S.A. 100, 7931-7936.
113. Rushworth, M. F., and Behrens, T. E. (2008). Choice, uncertainty and valuein prefrontal and cingulate cortex. Nat. Neurosci. 11, 389-397.
114. Rutishauser, U., Ross, I. B., Marmelak, A. N., and Schuman, E. M. (2010).Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903-907.
115. Sammer, G., Blecker, C., Gebhardt, H., Bischoff, M., Stark, R., Morgen, K., and Vaitl, D. (2007). Relationship between regional hemodynamic activity and simultaneously recorded EEG-theta associated with mental arithmeticinduced workload. Hum. Brain Mapp.28, 793-803.
116. Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., and von Stein, A. (1998). Synchronization betweenprefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. U.S.A. 95, 7092-7096.
117. Sauseng, P., Griesmayr, B., Freunberger, R., and Klimesch, W. (2009a). Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci. Biobehav. Rev. 34, 1015-1022.
118. Sauseng, P., Klimesch, W., Heise, K. F., Gruber, W. R., Holz, E., Karim, A. A., Glennon, M., Gerloff, C., Birbaumer, N., and Hummel, F. C. (2009b). Brain oscillatory substrates of visual shortterm memory capacity. Curr. Biol. 19, 1846-1852.
119. Schultz, W., Apicella, P., Scarnati, E., and Ljungberg, T. (1992). Neuronal activityin monkey ventral striatum related to the expectation of reward. J. Neurosci. 12, 4595-4610.
120. Sederberg, P. B., Kahana, M. J., Howard, M. W., Donner, E. J., and Madsen, J. R. (2003). Theta and gamma oscillations during encoding predict subsequentrecall. J. Neurosci. 23, 10809-10814.
121. Seidenbecher, T., Laxmi, T. R., Stork, O., and Pape, H. C. (2003). Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301, 846-850.
122. Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J., and Csicsvari, J. (2008). Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 28, 2274-2286.
123. Sharott, A., Moll, C. K., Engler, G., Denker, M., Grun, S., and Engel, A. K. (2009).Different subtypes of striatal neurons are selectively modulated bycortical oscillations. J. Neurosci. 29, 4571-4585.
124. Shima, K., and Tanji, J. (1998). Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282, 1335-1338.
125. Siapas, A. G., Lubenov, E. V., and Wilson, M. A. (2005). Prefrontal phase lockingto hippocampal theta oscillations. Neuron 46, 141-151.
126. Siegel, M., Warden, M. R., and Miller, E. K. (2009). Phase-dependent neuronalcoding of objects in short-term memory. Proc. Natl. Acad. Sci. U.S.A. 106, 21341-21346.
127. Singer, W. (2009). Distributed processing and temporal codes in neuronal networks. Cogn. Neurodyn. 3, 189-196.
128. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., and Buzsaki, G. (2008). Entrainment of neocortical neurons and gamma oscillationsby the hippocampal theta rhythm. Neuron 60, 683-697.
129. Steinvorth, S., Wang, C., Ulbert, I., Schomer, D., and Halgren, E.(2010). Human entorhinal gamma and theta oscillations selective forremote autobiographical memory. Hippocampus 20, 166-173.
130. Stewart, M., and Fox, S. E. (1990). Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci. 13, 163-168.
131. Summerfield, C., and Mangels, J. A. (2005). Coherent theta-band EEGactivity predicts item-context binding during encoding. Neuroimage 24, 692-703.
132. Tabuchi, E. T., Mulder, A. B., and Wiener, S. I. (2000). Position and behavioralmodulation of synchronization of hippocampal and accumbens neuronaldischarges in freely moving rats. Hippocampus 10, 717-728.
133. Talk, A., Kang, E., and Gabriel, M. (2004). Independent generation of theta rhythm in the hippocampus andposterior cingulate cortex. Brain Res. 1015, 15-24.
134. Traub, R. D., Miles, R., and Buzsaki, G. (1992). Computer simulation of carbachol- driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus. J. Physiol. 451, 653-672.
135. Tsujimoto, T., Shimazu, H., and Isomura, Y. (2006). Direct recording of theta oscillations in primate prefrontaland anterior cingulate cortices. J. Neurophysiol. 95, 2987-3000.
136. Tsujimoto, T., Shimazu, H., Isomura, Y., and Sasaki, K. (2010). Theta oscillations in primate prefrontal and anterior cingulate cortices in forewarnedreaction time tasks. J. Neurophysiol. 103, 827-843.
137. van der Meer, M. A., and Redish, A. D. (2009). Covert expectation-of-reward in rat ventral striatum at decision points. Front. Integr. Neurosci. 3:1. doi: 10.3389/neuro.07.001.2009.
138. van Wingerden, M., Vinck, M., Lankelma, J., and Pennartz, C. M. (2010). Thetabandphase locking of orbitofrontalneurons during reward expectancy. J. Neurosci. 30, 7078-7087.
139. Vinck, M., van Wingerden, M.,Womelsdorf, T., Fries, P., and Pennartz, C. M. (2010). The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. Neuroimage 51, 112-122.
140. von Stein, A., and Sarnthein, J. (2000). Different frequencies for differentscales of cortical integration: fromlocal gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 38, 301-313.
141. Wallis, J. D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30, 31-56.
142. Wang, X. J. (2008). Decision making in recurrent neuronal circuits. Neuron 60, 215-234.
143. Wang, X. J. (2010). Neurophysiological and computational principles of corticalrhythms in cognition. Physiol. Rev. 90, 1195-1268.
144. Watanabe, M. (2007). Role of anticipated reward in cognitive behavioral control. Curr. Opin. Neurobiol. 17, 213-219.
145. Wierzynski, C. M., Lubenov, E. V., Gu, M., and Siapas, A. G. (2009). Statedependentspike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61, 587-596.
146. Williams, Z. M., Bush, G., Rauch, S. L., Cosgrove, G. R., and Eskandar, E. N.(2004). Human anterior cingulated neurons and the integration of monetaryreward with motor responses. Nat. Neurosci. 7, 1370-1375.
147. Womelsdorf, T., and Fries, P. (2009). Selectiveattention through selective synchronization, in The Cognitive Neurosciences, edM. Gazzaniga (Cambridge, MA: MIT Press), 289-303.
148. Womelsdorf, T., Johnston, K., Vinck, M., and Everling, S. (2010). Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors. Proc. Natl. Acad. Sci. U.S.A. 107, 5248-5253.
149. Womelsdorf, T., Schoffelen, J. M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., and Fries, P. (2007). Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609-1612.
150. Woodnorth, M. A., Kyd, R. J., Logan, B. J., Long, M. A., and McNaughton, N.(2003). Multiple hypothalamic sitescontrol the frequency of hippocampaltheta rhythm. Hippocampus 13,361-374.
151. Wyart, V., and Tallon-Baudry, C. (2009). How ongoing fluctuations in humanvisual cortex predict perceptual awareness: baseline shift versus decision bias. J. Neurosci. 29, 8715-8725.
152. Young, C. K., and McNaughton, N. (2009). Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb. Cortex 19, 24-40.
153. Zilli, E. A., and Hasselmo, M. E. (2008). Modeling the role of working memory and episodic memory in behavioral tasks. Hippocampus 18, 193-209.