Increased entorhinal-prefrontal theta synchronization parallels decreased entorhinal-hippocampal theta synchronization during learning and consolidation of associative memory

Frontiers in Behavioral Neuroscience

Volumn , Issue JANUARY 2012, 2012, Pages

  Takehara Nishiuchi, Kaori ^a   Maal Bared, Geith ^a   Morrissey, Mark D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Consolidation; EEG; Episodic memory; Rats; Trace conditioning

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATIVE MEMORY; AUDITORY STIMULATION; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; ENTORHINAL CORTEX; EPISODIC MEMORY; EVOKED AUDITORY RESPONSE; EYELID REFLEX; HIPPOCAMPUS THETA RHYTHM; LEARNING; MALE; MEMORY CONSOLIDATION; NONHUMAN; PREFRONTAL CORTEX; RAT;

EID: 84856966357     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00090     Document Type: Article

References (73)

1. Agster, K. L., and Burwell, R. D. (2009). Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Hippocampus 19, 1159-1186.
2. Alonso, A., and Garcia-Austt, E. (1987a). Neuronal sources of theta rhythm in the entorhinal cortex of the rat. I. Laminar distribution of theta field potentials. Exp. Brain Res. 67, 493-501.
3. Alonso, A., and Garcia-Austt, E. (1987b). Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Exp. Brain Res. 67, 502-509.
4. Anderson, K. L., Rajagovindan, R., Ghacibeh, G. A., Meador, K. J., and Ding, M. (2010). Theta oscillations mediate interaction between pre- frontal cortex and medial temporal lobe in human memory. Cereb. Cortex 20,1604-1612.
5. Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., and Wiener, S. I. (2010). Coherent theta uoscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66, 921-936.
6. Berry, S. D., and Swain, R. A. (1989). Water deprivation optimizes hippocampal activity and facilitates nictitating membrane conditioning. Behav. Neurosci. 103, 71-76.
7. Berry, S. D., and Thompson, R. F. (1978). Prediction of learning rate from the hippocampal electroencephalogram. Science 200, 1298-1300.
8. Buzsaki, G.(2006). Rhythms ofthe Brain. NewYork: Oxford University Press.
9. Canto, C. B., Wouterlood, F. G., and Witter, M. P. (2008). What does the anatomical organization of the entorhinal cortex tell us? Neural Plast. 2008, 381243.
10. Darling, R. D., Takatsuki, K., Griffin, A. L., and Berry, S. D. (2011). Eye- blink conditioning contingent on hippocampal theta enhances hippocampal and medial prefrontal responses. J. Neurophysiol. 105, 2213-2224.
11. De Clercq, W., Lemmerling, P., Van Paesschen, W., and Van Huffel, S. (2003). Characterization of inter- ictal and ictal scalp EEG signals with the Hilbert transform. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1, 2459-2462.
12. Deshmukh, S. S., Yoganarasimha, D., Voicu, H., and Knierim, J. J. (2010). Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 104, 994-1006.
13. Eichenbaum, H. (2000). A cortical- hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41-50.
14. Fell, J., and Axmacher, N. (2011). The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12,105-118.
15. Fernandez, G., and Tendolkar, I. (2006). The rhinal cortex: "gatekeeper" of the declarative memory system. Trends Cogn. Sci. (Regul. Ed.) 10, 358-362.
16. Frankland, P. W., and Bontempi, B. (2005). The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119-130.
17. Galvez, R., Weiss, C., Weible, A. P., and Disterhoft, J. F. (2006). Vibrissa-signaled eyeblink conditioning induces somatosensory cortical plasticity. J. Neurosci. 26, 6062-6068.
18. Griffin, A. L., Asaka, Y., Darling, R. D., and Berry, S. D. (2004). Theta- contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav. Neu- rosci. 118,403-411.
19. Hoffmann, L. C., and Berry, S. D. (2009). Cerebellar theta oscillations are synchronized during hippocampal theta-contingent trace conditioning. Proc. Natl. Acad. Sci. U.S.A. 106,21371-21376.
20. Inda, M. C., Delgado-Garcia, J. M., and Carrion, A. M. (2005). Acquisition, consolidation, reconsolidation, and extinction of eyelid conditioning responses require de novo protein synthesis. J. Neurosci. 25, 2070-2080.
21. Jones, B. F., and Witter, M. P. (2007). Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17, 957-976.
22. Jones, M. W., and Wilson, M. A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoSBiol. 3,e402. doi:10.1371/jour- nal.pbio.0030402
23. Kalmbach, B. E., Ohyama, T., Kreider, J. C., Riusech, F., and Mauk, M. D. (2009). Interactions between prefrontal cortex and cerebellum revealed by trace eyelid conditioning. Learn. Mem. 16, 86-95.
24. Kerr, K. M., Agster, K. L., Furtak, S. C., and Burwell, R. D. (2007). Functional neuroanatomy of the parahip- pocampal region: the lateral and medial entorhinal areas. Hippocampus 17, 697-708.
25. Kim, J. J., Clark, R. E., and Thomp-Son, R. F. (1995).Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eye- blink conditioned responses. Behav. Neurosci. 109, 195-203.
26. Klimesch, W., Sauseng, P., and Gruber, W. (2009). The functional relevance of phase reset: a comment to Ris- ner et al. (2009): the visual evoked potential of surface alpha rhythm phase. Neuroimage 47, 5-7.
27. Kronforst-Collins, M. A., and Dister- hoft, J. F. (1998). Lesions of the caudal area of rabbit medial prefrontal cortex impair trace eyeblink conditioning. Neurobiol. Learn. Mem. 69, 147-162.
28. Lachaux, J. P., Rodriguez, E., Martinerie, J., and Varela, F. J. (1999). Measuring phase synchronyin brain signals. Hum. Brain Mapp. 8, 194-208.
29. Le Van Quyen, M., Foucher, J., Lachaux, J., Rodriguez, E., Lutz, A., Martinerie, J., and Varela, F. J. (2001). Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J. Neurosci. Methods 111, 83-98.
30. Lesburgueres, E., Gobbo, O. L., Alaux- Cantin, S., Hambucken, A., Trifil- ieff, P., and Bontempi, B. (2011). Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331,924-928.
31. Makinen, V., Tiitinen, H., and May, P. (2005). Auditory event-related responses are generated independently of ongoing brain activity. Neuroimage 24, 961-968.
32. Maviel, T., Durkin, T. P., Menzaghi, and Bontempi, B. (2004). Sites of neocortical reorganization critical for remote spatial memory. Science 305, 96-99.
33. McClelland, J. L., McNaughton, B. L., and O'reilly, R. C.(1995).Whythere are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102,419-457.
34. McLaughlin, J., Skaggs, H., Church- well, J., and Powell, D. A. (2002). Medial prefrontal cortex and Pavlov- ian conditioning: trace versus delay conditioning. Behav. Neurosci. 116, 37-47.
35. Miller, M. J., Weiss, C., Song, X., Iordanescu, G., Disterhoft, J. F., and Wyrwicz, A. M. (2008). Functional magnetic resonance imaging of delay and trace eyeblink conditioning in the primary visual cortex of the rabbit. J. Neurosci. 28, 4974-4981.
36. Mitzdorf, U. (1985). Current source- density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37-100.
37. Moyer, J. R. Jr., Deyo, R. A., and Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci. 104, 243-252.
38. Munera, A., Gruart, A., Munoz, M. D., Fernandez-Mas, R., and Delgado- Garcia, J. M. (2001). Hippocampal pyramidal cell activity encodes conditioned stimulus predictive value during classical conditioning in alert cats. J. Neurophysiol. 86, 2571-2582.
39. Nunez, P. L., and Srinivasan, R. (2006). Electric Fields ofthe Brain. NewYork: Oxford University Press.
40. Oswald, B. B., Maddox, S. A., Tisdale, N., and Powell, D. A. (2010). Encoding and retrieval are differentially processed by the anterior cingulate and prelimbic cortices: a study based on trace eyeblink conditioning in the rabbit. Neurobiol. Learn. Mem. 93, 37-45.
41. Paxinos, G., and Watson, C. (1986). The RatBrain in Stereotaxic Coordinates, 2nd Edn. San Diego: Academic Press.
42. Paz, R., Bauer, E. P., and Pare, D. (2008). Theta synchronizes the activity of medial prefrontal neurons during learning. Learn. Mem. 15, 524-531.
43. Restivo, L., Vetere, G., Bontempi, B., and Ammassari-Teule, M. (2009). The formation of recent and remote memory is associated with time- dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J. Neurosci. 29, 8206-8214.
44. Ross, R. S., and Eichenbaum, H. (2006). Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J. Neurosci. 26, 4852-4859.
45. Rudy, J. W., and O'Reilly, R. C. (2001). Conjunctive representations, the hippocampus, and contextual fear conditioning. Cogn. Affect. Behav. Neurosci. 1, 66-82.
46. Ryou, J. W., Cho, S. Y., and Kim, H. T. (2001). Lesions of the entorhi- nal cortex impair acquisition of hippocampal-dependent trace conditioning. Neurobiol. Learn. Mem. 75, 121-127.
47. Sacco, T., and Sacchetti, B. (2010). Role of secondary sensory cortices in emotional memory storage and retrieval in rats. Science 329, 649-656.
48. Sainsbury, R. S., Heynen, A., and Montoya, C. P. (1987). Behavioral correlates of hippocampal type 2 theta in the rat. Physiol. Behav. 39, 513-519.
49. Scoville, W. B., and Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatr. 20, 11-21.
50. Seager, M. A., Johnson, L. D., Chabot, E. S., Asaka, Y., and Berry, S. D. (2002). Oscillatory brain states and learning: impact of hippocampal theta- contingent training. Proc. Natl. Acad. Sci. U.S.A. 99, 1616-1620.
51. 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.
52. Siegel, J. J., Kalmbach, B., Chitwood, R. A., and Mauk, M. D. (2011). Persistent activity in a cortical-to- subcortical circuit: bridging the temporal gap in trace eyelid conditioning. J. Neurophysiol. [Epub ahead of print].
53. Simon, B., Knuckley, B., Churchwell, J., and Powell, D. A. (2005). Posttraining lesions of the medial pre- frontal cortex interfere with subsequent performance of trace eye- blink conditioning. J. Neurosci. 25, 10740-10746.
54. Singer, W. (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 55, 349-374.
55. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M, and Buzsaki, (2008). Entrainment of neocorti- cal neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697.
56. Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F., and Weisz, D. J. (1986). Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100, 729-744.
57. Squire, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195-231.
58. Squire, L.R., and Alvarez, P.(1995).Ret- rograde amnesia and memory consolidation: a neurobiological perspective. Curr. Opin. Neurobiol. 5, 169-177.
59. Takashima, A., Petersson, K. M., Rutters, F., Tendolkar, I., Jensen, O., Zwarts, M. J., McNaughton, B. L., and Fernandez, G. (2006). Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc. Natl. Acad. Sci. U.S.A. 103, 756-761.
60. Takehara, K., Kawahara, S., and Kirino, Y. (2003). Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J. Neu- rosci. 23, 9897-9905.
61. Takehara, K., Kawahara, S., Takatsuki, K., and Kirino, Y. (2002). Time- limited role of the hippocampus in the memory for trace eyeblink conditioning in mice. Brain Res. 951, 183-190.
62. Takehara-Nishiuchi, K., Kawahara, S., and Kirino, Y. (2005). NMDA receptor-dependent processes in the medial prefrontal cortex are important for acquisition and the early stage of consolidation during trace, but not delay eyeblink conditioning. Learn. Mem. 12, 606-614.
63. Takehara-Nishiuchi, K., and McNaughton, B. L. (2008). Spontaneous changes of neocortical code for associative memory during consolidation. Science 322, 960-963.
64. Takehara-Nishiuchi, K., Nakao, K., Kawahara, S., Matsuki, N., and Kirino, Y. (2006). Systems consolidation requires postlearning activation of NMDA receptors in the medial prefrontal cortex in trace eye- blink conditioning. J. Neurosci. 26, 5049-5058.
65. Teyler, T. J., and DiScenna, P. (1986). The hippocampal memory indexing theory. Behav. Neurosci. 100, 147-154.
66. Varela, F., Lachaux, J. P., Rodriguez, E., and Martinerie, J. (2001). The brain- web: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229-239.
67. Vetere, G., Restivo, L., Cole, C. J., Ross, P. J., Ammassari-Teule, M., Josselyn, S. A., and Frankland, P. W. (2011). Spine growth in the anterior cingu- late cortex is necessary for the consolidation of contextual fear memory. Proc. Natl.Acad. Sci. U.S.A. 108, 8456-8460.
68. Weible, A. P., McEchron, M. D., and Disterhoft, J. F. (2000). Cortical involvement in acquisition and extinction of trace eyeblink conditioning. Behav. Neurosci. 114, 1058-1067.
69. Weiss, C., Bouwmeester, H., Power, J. M., and Disterhoft, J. F. (1999). Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav. Brain Res. 99, 123-132.
70. Wikgren, J., Nokia, M. S., and Pent- tonen, M. (2010). Hippocampo- cerebellar theta band phase synchrony in rabbits. Neuroscience 165, 1538-1545.
71. Womelsdorf, T., Schoffelen, J. M., Oost- enveld, R., Singer, W., Desimone, R., Engel, A. K., and Fries, P. (2007). Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609-1612.
72. Yasuda, M., and Mayford, M. R. CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron 50, 309-318.
73. Young, B. J., Otto, T., Fox, G. D., and Eichenbaum, H. (1997). Memory representation within the parahip- pocampal region. J. Neurosci. 17, 5183-5195.