What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms?

Frontiers in Neuroscience

Volumn , Issue MAR, 2011, Pages

  Hyman, James Michael ^a   Hasselmo, Michael Erik ^b   Seamans, Jeremy Keith ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BOSTON UNIVERSITY   (United States)

Author keywords

Hippocampus; Oscillations; Prefrontal cortex; Theta rhythm; Working memory

Indexed keywords

ANTIDROMIC STIMULATION; ATTENTION; BEHAVIOR CHANGE; HIPPOCAMPUS THETA RHYTHM; HUMAN; HUMAN CELL; INFORMATION PROCESSING; NERVE CELL; OSCILLATION; OUTCOME ASSESSMENT; PREFRONTAL CORTEX; REVIEW; TASK PERFORMANCE; WORKING MEMORY;

EID: 79960627489     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2011.00024     Document Type: Review

References (79)

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. Anderson, K. L., Rajagovindan, R., Ghacibeh, G. A., Meador, K. J., and Ding, M. (2010). Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb. Cortex 20, 1604-1612.
3. Asada, H., Fukuda, Y., Tsunoda, S., Yamaguchi, M., and Tonoike, M. (1999). Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulate cortex in humans. Neurosci. Lett. 274, 29-32.
4. Başar, E. (1980). EEG Brain Dynamics: Relation Between EEG and Brain Evoked Potentials. Amsterdam: Elsevier.
5. Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., 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.
6. Botvinick, M. M. (2007). Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function. Cogn. Affect. Behav. Neurosci. 7, 356-366.
7. Brazhnik, E. S., Vinogradova, O. S., and Karanov, A. M. (1985). Frequency modulation of neuronal theta-bursts in rabbit's septum by low-frequency repetitive stimulation of the afferent pathways. Neuroscience 14, 501-508.
8. Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: Anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1-38.
9. 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.
10. Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., and Cohen, J. D. (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280, 747-749.
11. Cavanaugh, J. F., Cohen, M. X., and Allen, J. J. B. (2009). Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J. Neurosci. 29, 98-105.
12. Cavanaugh, J. F., Frank, M. J., Klein, T. J., and Allen, J. J. B. (2010). Frontal theta links prediction errors to behavioral adaptation in reinforcement learning. Neuroimage 49, 3198-3209.
13. Cowen, S. L., and McNaughton, B. L. (2007). Selective delay activity in the medial prefrontal cortex of the rat: Contribution of sensorimotor information and contingency. J. Neurophysiol. 98, 303-316.
14. Delorme, A., Westerfield, M., and Makeig, S. (2007). Medial prefrontal theta bursts precede rapid motor responses during visual selective attention. J. Neurosci. 27, 11949-11959.
15. Durstewitz, D., Vittoz, N. M., Floresco, S. B., and Seamans, J. K. (2010). Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron 66, 438-448.
16. Eichele, T., Debener, S., Calhoun, V. D., Specht, K., Engel, A. K., Hugdahi, K., von Cramon, D. Y., and Ullsperger, M. (2008). Prediction of human errors by maladaptive changes in event-related brain networks. Proc. Natl. Acad. Sci. U.S.A. 105, 6173-6178.
17. Eichenbaum, H. (2004). Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109-120.
18. Ekstrom, A. D., Caplan, J. B., Ho, E., Shattuck, K., Fried, I., and Kahana, M. J. (2005). Human hippocampal theta activity during virtual navigation. Hippocampus 15, 881-889.
19. Euston, D. R., and McNaughton, B. L. (2006). Apparent encoding of sequential context in rat medial prefrontal cortex is accounted for by behavioral variability. J. Neurosci. 26,13143-13155.
20. Gemmell, C., Anderson, M., and O'Mara, S. M. (2002). Deep layer prefrontal cortex unit discharge in a cue-controlled open-field environment in the freely-moving rat. Behav. Brain Res. 133, 1-10.
21. 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.
22. Givens, B. (1996). Stimulus-evoked resetting of the dentate theta rhythm: Relation to working memory. Neuroreport 8, 159-163.
23. Hampson, R. E., and Deadwyler, S. A. (1996). Ensemble codes involving hippocampal neurons are at risk during delayed performance tests. Proc. Natl. Acad. Sci. U.S.A. 93, 13487-13493.
24. Hampson, R. E., Heyser, C. J., and Deadwyler, S. A. (1993). Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav. Neurosci. 107, 715-739.
25. Hanslmayr, S., Pastötter, B., Bäuml, K., Gruber, S., Wimber, M., and Klimesch, W. (2008). The electrophysiological dynamics of interference during the Stroop task. J. Cogn. Neurosci. 20, 215-225.
26. Hasselmo, M. E. (2007). Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function. Learn. Mem. 14, 782-794.
27. Hasselmo, M. E. (2008). Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213-1229.
28. Hastie, T., Tibshirani, R., and Friedman, J. (2009). The Elements of Statistical Learning: Data Mining, Inference, and Prediction. New York: Springer Science.
29. Hok, V., Save, E., Lenck-Santini, P. P., and Poucet, B. (2005). Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc. Natl. Acad. Sci. U.S.A. 102, 4602-4607.
30. 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.
31. Hyman, J. M., Zilli, E. A., Paley, A. M., and Hasselmo, M. E. (2010). Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front. Integr. Neurosci. 4:2. doi: 10.3389/neuro.07.002.2010
32. 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.
33. Ito, S., Stuphorn, V., Brown, J. W., and Schall, J. D. (2003). Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120-122.
34. Jensen, O., and Lisman, J. E. (1996). Hippocampal CA3 region predicts memory sequences: Accounting for the phase precession of place cells. Learn. Mem. 3, 264-278.
35. Jensen, O., and Tesche, C. D. (2002). Frontal theta activity in humans increases with memory load in a working memory task. Eur. J. Neurosci. 15, 1395-1399.
36. 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
37. 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.
38. Jung, M. W., Qin, Y., McNaughton, B. L., and Barnes, C. A. (1998). Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb. Cortex 8, 437-450.
39. Kahana, M. J., Seelig, D., and Madsen, J. R. (2001). Theta returns. Curr. Opin. Neurobiol. 11, 739-744.
40. Kahana, M. J., Sekuler, R., Caplan, J. B., Kirschen, M., and Madsen, J. R. (1999). Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399, 781-784.
41. Klimesch, W., Schack, B., Schabus, M., Doppelmayr, M., Gruber, W., and Sauseng, P. (2004). Phase-locked alpha and theta oscillations generate the p1-n1 complex and are related to memory performance. Brain Res. Cogn. Brain Res. 19, 302-316.
42. Kramis, R., Vanderwolf, C. H., and Bland, B. H. (1975). Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relation to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 49, 58-85.
43. Krzanowski, W. J. (2000). Principles of Multivariate Analysis: A User's Perspective. New York: Oxford University Press.
44. Lapish, C. C., Durstewitz, D., Chandler, L. J., and Seamans, J. K. (2008). Successful choice behavior is associated with distinct and coherent network states in anterior cingulate cortex. Proc. Natl. Acad. Sci. U.S.A. 105, 11963-11968.
45. Laroche, S., Davis, S., Jay, T. M., and Thierry, A. M. (1990). Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci. Lett. 114, 184-190.
46. Marco-Pallarés, J., Camara, E., Münte, T. F., and Rodríguez-Fornells, A. (2008). Neural mechanisms underlying adaptive actions after slips. J. Cogn. Neurosci. 20, 1595-1610.
47. McCartney, H., Johnson, A. D., Weil, Z. M., and Givens, B. (2004). Theta reset produces optimal conditions for long-term potentiation. Hippocampus 14, 684-687.
48. Meltzer, J. A., Negishi, M., Mayes, L. C., and Constable, R. T. (2007). Individual differences in EEG theta and alpha dynamics during working memory correlate with fMRI responses across subjects. Clin. Neuropsychol. 118, 2419-2436.
49. 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.
50. Miller, E. K., Freedman, D. J., and Wallis, J. D. (2002). The prefrontal cortex: categories, concepts and cognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1123-1136.
51. Miller, R. (1991). Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain. (Studies in brain function no. 17). Berlin: Springer.
52. Mizuhara, H., Wang, L. Q., Kobayashi, K., and Yamaguchi, Y. (2004). A long-range cortical network emerging with theta oscillation in a mental task. Neuroreport 15, 1233-1238.
53. Mizuhara, H., and Yamaguchi, Y. (2007). Human cortical circuits for central executive function emerge by theta phase synchronization. Neuroimage 36, 232-244.
54. Narayanan, N. S., and Laubach, M. (2006). Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron 7, 921-931.
55. Narayanan, N. S., and Laubach, M. (2008). Neuronal correlates of post-error slowing in the rat dorsomedial prefrontal cortex. J. Neurophysiol. 100, 520-525.
56. Narayanan, N. S., and Laubach, M. (2009). Delay activity in rodent frontal cortex during a simple reaction time task. J. Neurophysiol. 101, 2859-2871.
57. O'Keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175.
58. O'Keefe, J., and Recce, M. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330.
59. Onton, J., Delorme, A., and Makeig, S. (2005). Frontal midline EEG dynamics during working memory. Neuroimage 27, 341-356.
60. Poucet, B. (1998). Searching for spatial unit firing in the prelimbic area of the rat medial prefrontal cortex. Behav. Brain Res. 84, 151-159.
61. 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 human theta oscillations by a working memory task. J. Neurosci. 21, 3175-3183.
62. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
63. Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., and von Stein, A. (1998). Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. U.S.A. 95, 7092-7096.
64. Sarnthein, J., Stern, J. Aufenberg, C., Rousson, V., and Jeanmonod, D. (2006). Increased EEG power and slowed dominant frequency in patients with neurogenic pain. Brain 129, 55-64.
65. Sasaki, K., Nambu, A., Tsujimoto, T., Matsuzaki, R., Kyuhou, S., and Gemba, H. (1996). Studies on integrative functions of the human frontal association cortex with MEG. Brain Res. Cogn. Brain Res. 5, 165-174.
66. Sauseng, P., Klimesch, W., Freunberger, R., Pecherstorfer, T., Hanslmayr, S., and Doppelmayr, M. (2006). Relevance of EEG alpha and theta oscillations during task switching. Exp. Brain Res. 170, 295-301.
67. Seamans, J. K., Hyman, J. M., Lapish, C. C., Balaguer-Ballester, E., Ma, L., and Durstewitz, D. (2009). A prefrontal cortex network representation of mental set in rats. Abstr. Soc. Neurosci. 579.9.
68. Siapas, A. G., Lubenov, E. V., and Wilson, M. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151.
69. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., and Buzsaki, G. (2008). Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697.
70. Tesche, C. D., and Karhu, J. (2000). Theta oscillations index human hippocampal activation during a working memory task. Proc. Natl. Acad. Sci. U.S.A. 97, 919-924.
71. van Veen, V., and Carter, C. S. (2002). The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiol. Behav. 77, 477-482.
72. Vertes, R. P. (2006). Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142, 1-20.
73. Vinogradova, O. S., Brazhnik, E. S., Kitchigina, V. F., and Stafekhina, V. S. (1993). Acetylcholine, theta-rhythm and activity of hippocampal neurons in the rabbit-IV: Sensory stimulation. Neuroscience 53, 993-1007.
74. Vogt, B. A., and Vogt, L. (2003). Cytology of human dorsal midcingulate and supplementary motor cortices. J. Chem. Neuroanat. 26, 301-309.
75. von Stein, A., and Sarnthein, J. (2000). Different frequencies for different scales of cortical integration: From local gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 38, 301-313.
76. Wang, C., Ulbert, I., Schomer, D. L., Marinkovic, K., and Halgren, E. (2005). Responses of human anterior cingulate cortex microdomains to error detection, conflict monitoring, stimulus-response mapping, familiarity, and orienting. J. Neurosci. 25, 604-613.
77. Weissman, D. H., Roberts, K. C., Visscher, K. M., and Woldorff, M. G. (2006). The neural bases of momentary lapses in attention. Nat. Neurosci. 9, 971-978.
78. Williams, J. M., and Givens, B. (2003). Stimulation-induced reset of hippocampal theta in the freely performing rat. Hippocampus 13, 109-116.
79. Wilson, M. A., and McNaughton, B. L. (1993). Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058.