Updating hippocampal representations: CA2 joins the circuit

Trends in Neurosciences

Volumn 34, Issue 10, 2011, Pages 526-535

  Jones, Matthew W ^a   Mchugh, Thomas J ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN ELECTROPHYSIOLOGY; DEGENERATIVE DISEASE; ENTORHINAL CORTEX; EPILEPSY; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; MEMORY; MEMORY CONSOLIDATION; NERVE PROJECTION; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECALL; REVIEW; SCHIZOPHRENIA; THINKING;

ANIMALS; CA2 REGION, HIPPOCAMPAL; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NERVE NET;

EID: 80053125882     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2011.07.007     Document Type: Review

References (135)

1. Willshaw D.J., Buckingham J.T. An assessment of Marr's theory of the hippocampus as a temporary memory store. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1990, 329:205-215.
2. McNaughton B.L., Morris R.G. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 1987, 10:408-415.
3. McClelland J.L., et al. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 1995, 102:419-457.
4. Lisman J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 1999, 22:233-242.
5. Rolls E.T. A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 2010, 215:180-196.
6. Yassa M.A., Stark C.E.L. Pattern separation in the hippocampus. Trends Neurosci. 2011, 34:515-525.
7. Clayton N.S., et al. Episodic memory. Curr. Biol. 2007, 17:R189-R191.
8. Nakazawa K., et al. Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 2003, 38:305-315.
9. Zentall T.R., et al. Episodic-like memory in pigeons. Psychon. Bull. Rev. 2001, 8:685-690.
10. Morris R.G. Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2001, 356:1453-1465.
11. Lipton P.A., Eichenbaum H. Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural. Plas. 2008, 2008:258467.
12. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press.
13. Morris R.G., et al. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
14. O'Keefe J., Conway D.H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 1978, 31:573-590.
15. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
16. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
17. Eichenbaum H., et al. The hippocampus, memory, and place cells: is it spatial memory or a memory space?. Neuron 1999, 23:209-226.
18. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
19. Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001, 29:145-156.
20. Poucet B., et al. Sensory and memory properties of hippocampal place cells. Rev. Neurosci. 2000, 11:95-111.
21. Moser E.I., Paulsen O. New excitement in cognitive space: between place cells and spatial memory. Curr. Opin. Neurobiol. 2001, 11:745-751.
22. Pastalkova E., et al. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
23. Ekstrom A.D., et al. Cellular networks underlying human spatial navigation. Nature 2003, 425:184-188.
24. Quiroga R.Q., et al. Sparse but not 'grandmother-cell' coding in the medial temporal lobe. Trends Cogn. Sci. 2008, 12:87-91.
25. Doeller C.F., et al. Evidence for grid cells in a human memory network. Nature 2010, 463:657-661.
26. Hafting T., et al. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
27. Moser E.I., et al. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 2008, 31:69-89.
28. Derdikman D., Moser E.I. A manifold of spatial maps in the brain. Trends Cogn. Sci. 2010, 14:561-569.
29. Sargolini F., et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
30. Taube J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 2007, 30:181-207.
31. Calton J.L., Taube J.S. Where am I and how will I get there from here? A role for posterior parietal cortex in the integration of spatial information and route planning. Neurobiol. Learn. Mem. 2009, 91:186-196.
32. Vann S.D., et al. What does the retrosplenial cortex do?. Nat. Rev. Neurosci. 2009, 10:792-802.
33. Solstad T., et al. Representation of geometric borders in the entorhinal cortex. Science 2008, 322:1865-1868.
34. Savelli F., et al. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 2008, 18:1270-1282.
35. Hargreaves E.L., et al. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
36. Yoganarasimha D., et al. Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 2010, 10.1002/hipo.20839.
37. Deshmukh S.S., et al. Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 2010, 104:994-1006.
38. Solstad T., et al. From grid cells to place cells: a mathematical model. Hippocampus 2006, 16:1026-1031.
39. Burgess N., et al. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
40. Molter C., Yamaguchi Y. Entorhinal theta phase precession sculpts dentate gyrus place fields. Hippocampus 2008, 18:919-930.
41. van Strien N.M., et al. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 2009, 10:272-282.
42. Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 2010, 66:560-572.
43. Beed P., et al. Analysis of excitatory microcircuitry in the medial entorhinal cortex reveals cell-type-specific differences. Neuron 2010, 68:1059-1066.
44. Lorente de No R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 1934, 46:113-177.
45. Magloczky Z., et al. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 1994, 4:322-334.
46. Soussi R., et al. Heterogeneity of the supramammillary-hippocampal pathways: evidence for a unique GABAergic neurotransmitter phenotype and regional differences. Eur. J. Neurosci. 2010, 32:771-785.
47. Wouterlood F.G., et al. Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 1990, 296:179-203.
48. Halasy K., et al. Distribution and origin of vesicular glutamate transporter 2-immunoreactive fibers in the rat hippocampus. Hippocampus 2004, 14:908-918.
49. Lein E.S., et al. Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. J. Comp. Neurol. 2005, 485:1-10.
50. Young W.S., et al. The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy. Neuroscience 2006, 143:1031-1039.
51. Ochiishi T., et al. High level of adenosine A1 receptor-like immunoreactivity in the CA2/CA3a region of the adult rat hippocampus. Neuroscience 1999, 93:955-967.
52. Bland S.T., et al. Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress. Neuroscience 2007, 144:1219-1228.
53. Lee S.E., et al. RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16994-16998.
54. Sekino Y., et al. Delayed signal propagation via CA2 in rat hippocampal slices revealed by optical recording. J. Neurophysiol. 1997, 78:1662-1668.
55. Bartesaghi R., Gessi T. Parallel activation of field CA2 and dentate gyrus by synaptically elicited perforant path volleys. Hippocampus 2004, 14:948-963.
56. Zhao M., et al. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J. Neurosci. 2007, 27:12025-12032.
57. Simons S.B., et al. Regional differences in hippocampal calcium handling provide a cellular mechanism for limiting plasticity. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14080-14084.
58. Mercer A., et al. Characterization of neurons in the CA2 subfield of the adult rat hippocampus. J. Neurosci. 2007, 27:7329-7338.
59. Mercer A., et al. Local circuitry involving parvalbumin-positive basket cells in the CA2 region of the hippocampus. Hippocampus 2010, 10.1002/hipo.20841.
60. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008, 9:206-221.
61. Takahashi H., Magee J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
62. Otmakhova N.A., Lisman J.E. Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J. Neurosci. 1999, 19:1437-1445.
63. Remondes M., Schuman E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416:736-740.
64. Hafting T., et al. Hippocampus-independent phase precession in entorhinal grid cells. Nature 2008, 453:1248-1252.
65. Wersinger S.R., et al. Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol. Psychiatry 2002, 7:975-984.
66. DeVito L.M., et al. Vasopressin 1b receptor knock-out impairs memory for temporal order. J. Neurosci. 2009, 29:2676-2683.
67. Martig A.K., Mizumori S.J. Ventral tegmental area disruption selectively affects CA1/CA2 but not CA3 place fields during a differential reward working memory task. Hippocampus 2011, 21:172-184.
68. Colgin L.L., et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
69. Hasselmo M.E. What is the function of hippocampal theta rhythm? Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005, 15:936-949.
70. Yeckel M.F., Berger T.W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:5832-5836.
71. Do V.H., et al. Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. J. Neurophysiol. 2002, 87:669-678.
72. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
73. Montgomery S.M., et al. Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J. Neurosci. 2009, 29:1381-1394.
74. Mizuseki K., et al. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 2009, 64:267-280.
75. Leutgeb S., et al. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 2004, 305:1295-1298.
76. Karlsson M.P., Frank L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J. Neurosci. 2008, 28:14271-14281.
77. Brun V.H., et al. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296:2243-2246.
78. Brun V.H., et al. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 2008, 57:290-302.
79. Nakashiba T., et al. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319:1260-1264.
80. Jeewajee A., et al. Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 2008, 18:340-348.
81. Pan W.X., McNaughton N. The supramammillary area: its organization, functions and relationship to the hippocampus. Prog. Neurobiol. 2004, 74:127-166.
82. Sekino Y., Shirao T. A role for signal propagation through the hippocampal CA2 field in memory formation. WImBI'06 Proceedings of the 1st WICI International Conference on Web Intelligence Meets Brain Informatics 2006, 254-266. Springer-Verlag. N. Zhong (Ed.).
83. Csicsvari J., et al. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28:585-594.
84. O'Neill J., et al. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010, 33:220-229.
85. Cheng S., Frank L.M. New experiences enhance coordinated neural activity in the hippocampus. Neuron 2008, 57:303-313.
86. Dupret D., et al. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 2010, 13:995-1002.
87. Nakashiba T., et al. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 2009, 62:781-787.
88. Porkka-Heiskanen T., Kalinchuk A.V. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev 2011, 15:123-135.
89. McDermott C.M., et al. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J Physiol 2006, 570:553-565.
90. Henriksen E.J., et al. Spatial representation along the proximodistal axis of CA1. Neuron 2010, 68:127-137.
91. Burke S.N., et al. The influence of objects on place field expression and size in distal hippocampal CA1. Hippocampus 2011, 21:783-801.
92. Lever C., et al. Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum. Hippocampus 2010, 20:229-234.
93. Lubenov E.V., Siapas A.G. Hippocampal theta oscillations are travelling waves. Nature 2009, 459:534-539.
94. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
95. Royer S., et al. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 2010, 30:1777-1787.
96. Kjelstrup K.B., et al. Finite scale of spatial representation in the hippocampus. Science 2008, 321:140-143.
97. Jovalekic A., et al. Horizontal biases in rats' use of three-dimensional space. Behav. Brain Res. 2011, 222:279-288.
98. Grobety M.-C., Schenk F. The influence of spatial irregularity upon radial-maze performance in the rat. Anim. Learn. Behav. 1992, 20:393-400.
99. Knierim J.J., McNaughton B.L. Hippocampal place-cell firing during movement in three-dimensional space. J. Neurophysiol. 2001, 85:105-116.
100. Adhikari A., et al. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010, 65:257-269.
101. de Hoz L., et al. Longitudinal axis of the hippocampus: both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus 2003, 13:587-603.
102. Witter M.P. Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. Learn. Mem. 2007, 14:705-713.
103. Li X.G., et al. The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 1994, 339:181-208.
104. Lein E.S., et al. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J. Neurosci. 2004, 24:3879-3889.
105. Dong H.W., et al. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11794-11799.
106. Lee A.K., et al. Head-anchored whole-cell recordings in freely moving rats. Nat. Protoc. 2009, 4:385-392.
107. Dombeck D.A., et al. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 2010, 13:1433-1440.
108. Epsztein J., et al. Impact of spikelets on hippocampal CA1 pyramidal cell activity during spatial exploration. Science 2010, 327:474-477.
109. Epsztein J., et al. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 2011, 70:109-120.
110. Deguchi Y., et al. Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat. Neurosci. 2011, 14:495-504.
111. Ewell L.A., Jones M.V. Frequency-tuned distribution of inhibition in the dentate gyrus. J. Neurosci. 2010, 30:12597-12607.
112. Tateno K., et al. Synchronized spike selection in a hippocampal dentate gyrus network model in the theta frequency range. International Congress Series 2007, 1301:79-82.
113. Akam T., Kullmann D.M. Oscillations and filtering networks support flexible routing of information. Neuron 2010, 67:308-320.
114. Nitz D., McNaughton B. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J. Neurophysiol. 2004, 91:863-872.
115. Heys J.G., et al. Cholinergic modulation of the resonance properties of stellate cells in layer II of medial entorhinal cortex. J. Neurophysiol. 2010, 104:258-270.
116. Acsady L., et al. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 1998, 18:3386-3403.
117. Bragin A., et al. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol. 1995, 73:1691-1705.
118. Henze D.A., et al. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 2002, 5:790-795.
119. Scharfman H.E. The CA3 'backprojection' to the dentate gyrus. Prog. Brain Res. 2007, 163:627-637.
120. Myers C.E., Scharfman H.E. Pattern separation in the dentate gyrus: a role for the CA3 backprojection. Hippocampus 2010, 10.1002/hipo.20828.
121. Dam A.M. Epilepsy and neuron loss in the hippocampus. Epilepsia 1980, 21:617-629.
122. Sloviter R.S. 'Epileptic' brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res. Bull. 1983, 10:675-697.
123. Van Dycke A., et al. Continuous local intrahippocampal delivery of adenosine reduces seizure frequency in rats with spontaneous seizures. Epilepsia 2010, 51:1721-1728.
124. Scorza C.A., et al. Distinctive hippocampal CA2 subfield of the Amazon rodent Proechimys. Neuroscience 2010, 169:965-973.
125. Cohen-Gadol A.A., et al. Mesial temporal lobe epilepsy: a proton magnetic resonance spectroscopy study and a histopathological analysis. J. Neurosurg. 2004, 101:613-620.
126. Brady D.R., Mufson E.J. Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain. Neuroscience 1997, 80:1113-1125.
127. Mueller S.G., et al. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum. Brain Mapp. 2010, 31:1339-1347.
128. Harrison P.J., Weinberger D.R. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry 2005, 10:40-68.
129. Benes F.M., et al. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol. Psychiatry 1998, 44:88-97.
130. Zhang Z., et al. A selective reduction in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia patients. Chin. Med. J. (Engl.) 2002, 115:819-823.
131. Knable M.B., et al. Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol. Psychiatry 2004, 9:609-620. 544.
132. Hashimoto T., et al. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am. J. Psychiatry 2008, 165:479-489.
133. Gao X.M., et al. Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am. J. Psychiatry 2000, 157:1141-1149.
134. Jin C.Y., et al. Altered histamine H3 receptor radioligand binding in post-mortem brain samples from subjects with psychiatric diseases. Br. J. Pharmacol. 2009, 157:118-129.
135. Narr K.L., et al. Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 2004, 21:1563-1575.