A single microcircuit with multiple functions: State dependent information processing in the hippocampus

Current Opinion in Neurobiology

Volumn 22, Issue 4, 2012, Pages 704-708

  Carr, Margaret F ^a   Frank, Loren M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL SCIENCE; BRAIN FUNCTION; BRAIN REGION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; LEARNING; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; TASK PERFORMANCE;

CA1 REGION, HIPPOCAMPAL; HUMANS; MENTAL PROCESSES; MODELS, NEUROLOGICAL; NERVE NET; NEURONS;

EID: 84866001607     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2012.03.007     Document Type: Review

References (49)

1. Karlsson M.P., Frank L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neurosci 2008, 28:14271-14281.
2. Frank L.M., Stanley G.B., Brown E.N. Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 2004, 24:7681-7689.
3. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
4. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
5. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 1999, 19:4090-4101.
6. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
7. Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 2009, 12:1222-1223.
8. Ego-Stengel V., Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 2010, 20:1-10.
9. Foster D.J., Wilson M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 2006, 440:680-683.
10. Diba K., Buzsaki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 2007, 10:1241-1242.
11. Gupta A.S., van der Meer M.A., Touretzky D.S., Redish A.D. Hippocampal replay is not a simple function of experience. Neuron 2010, 65:695-705.
12. Karlsson M.P., Frank L.M. Awake replay of remote experiences in the hippocampus. Nat Neurosci 2009, 12:913-918.
13. O'Neill J., Senior T., Csicsvari J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 2006, 49:143-155.
14. Cheng S., Frank L.M. New experiences enhance coordinated neural activity in the hippocampus. Neuron 2008, 57:303-313.
15. Dupret D., O'Neill J., Pleydell-Bouverie B., Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci 2010, 13:995-1002.
16. O'Neill J., Pleydell-Bouverie B., Dupret D., Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci 2010, 33:220-229.
17. Jadhav S.P., Kemere C., German P.W., Frank L.M. Awake hippocampal sharp-wave ripples support spatial memory. Science 2012, 336:1454-1458.
18. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31:571-591.
19. Fyhn M., Molden S., Witter M.P., Moser E.I., Moser M.B. Spatial representation in the entorhinal cortex. Science 2004, 305:1258-1264.
20. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
21. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.B., Moser E.I. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
22. Solstad T., Boccara C.N., Kropff E., Moser M.B., Moser E.I. Representation of geometric borders in the entorhinal cortex. Science 2008, 322:1865-1868.
23. Brun V.H., Leutgeb S., Wu H.Q., Schwarcz R., Witter M.P., Moser E.I., Moser M.B. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 2008, 57:290-302.
24. Suh J., Rivest A.J., Nakashiba T., Tominaga T., Tonegawa S. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 2011, 334:1415-1420.
25. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
26. Brun V.H., Otnass M.K., Molden S., Steffenach H.A., Witter M.P., Moser M.B., Moser E.I. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296:2243-2246.
27. Remondes M., Schuman E.M. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 2004, 431:699-703.
28. Vago D.R., Bevan A., Kesner R.P. The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval. Hippocampus 2007, 17:977-987.
29. Vago D.R., Kesner R.P. Disruption of the direct perforant path input to the CA1 subregion of the dorsal hippocampus interferes with spatial working memory and novelty detection. Behav Brain Res 2008, 189:273-283.
30. Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 2010, 66:560-572.
31. Jones M.W., McHugh T.J. Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci 2011, 34:526-535.
32. Nakazawa K., Sun L.D., Quirk M.C., Rondi-Reig L., Wilson M.A., Tonegawa S. Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 2003, 38:305-315.
33. Csicsvari J., Hirase H., Mamiya A., Buzsaki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28:585-594.
34. Sullivan D., Csicsvari J., Mizuseki K., Montgomery S., Diba K., Buzsaki G. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 2011, 31:8605-8616.
35. Nakashiba T., Buhl D.L., McHugh T.J., Tonegawa S. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 2009, 62:781-787.
36. Winson J., Abzug C. Neuronal transmission through hippocampal pathways dependent on behavior. J Neurophysiol 1978, 41:716-732.
37. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 1969, 26:407-418.
38. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K., Buzsaki G. Gamma (40-100Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 1995, 15:47-60.
39. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
40. Akam T., Kullmann D.M. Oscillations and filtering networks support flexible routing of information. Neuron 2010, 67:308-320.
41. Chen Z., Resnik E., McFarland J.M., Sakmann B., Mehta M.R. Speed controls the amplitude and timing of the hippocampal gamma rhythm. PLoS ONE 2011, 6:e21408.
42. Montgomery S.M., Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci U S A 2007, 104:14495-14500.
43. Niell C.M., Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 2010, 65:472-479.
44. Maimon G., Straw A.D., Dickinson M.H. Active flight increases the gain of visual motion processing in Drosophila. Nat Neurosci 2010, 13:393-399.
45. Mizuseki K., Diba K., Pastalkova E., Buzsaki G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat Neurosci 2011, 14:1174-1181.
46. Hasselmo M.E., Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 1994, 14:3898-3914.
47. Li S., Cullen W.K., Anwyl R., Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 2003, 6:526-531.
48. Singer A.C., Frank L.M. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 2009, 64:910-921.
49. Luo A.H., Tahsili-Fahadan P., Wise R.A., Lupica C.R., Aston-Jones G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 2011, 333:353-357.