Glutamate dysfunction in hippocampus: Relevance of dentate gyrus and CA3 signaling

Schizophrenia Bulletin

Volumn 38, Issue 5, 2012, Pages 927-935

  Tamminga, Carol A ^a   Southcott, Sarah ^a   Sacco, Carolyn ^a   Wagner, Anthony D ^b   Ghose, Subroto ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

CA1; CA3; dentate gyrus; glutamatergic transmission; metaplasticity; plasticity

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMIC ACID;

ANXIETY; ARTICLE; ASSOCIATION CORTEX; ASTROCYTE; BRAIN PERFUSION; DELUSION; DENTATE GYRUS; ENTORHINAL CORTEX; FUNCTIONAL NEUROIMAGING; HIPPOCAMPAL CA3 REGION; HUMAN; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; MENTAL STRESS; NEOCORTEX; NERVE CELL PLASTICITY; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PARAHIPPOCAMPAL GYRUS; PRIORITY JOURNAL; PSYCHOSIS; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TASK PERFORMANCE; TEMPORAL LOBE; THOUGHT DISORDER;

ANXIETY; AROUSAL; ASSOCIATION; BRAIN; CA3 REGION, HIPPOCAMPAL; DENTATE GYRUS; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; MEMORY; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84866682641     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbs062     Document Type: Article

References (99)

1. Benarroch EE. NMDA receptors: recent insights and clinical correlations. Neurology. 2011;76:1750-1757.
2. Nikam SS, Kornberg BE. AMPA receptor antagonists. Curr Med Chem. 2001;8:155-170.
3. Lynch DR, Guttmann RP. NMDA receptor pharmacology: perspectives from molecular biology. Curr Drug Targets. 2001;2:215-231.
4. Song I, Huganir RL. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 2002;25:578-588.
5. Lee MC, Yasuda R, Ehlers MD. Metaplasticity at single glutamatergic synapses. Neuron. 2010;66:859-870.
6. Shepherd JD, Huganir RL. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol. 2007;23:613-643.
7. Greer PL, Greenberg ME. From synapse to nucleus: calciumdependent gene transcription in the control of synapse development and function. Neuron. 2008;59:846-860.
8. Greer PL, Zieg J, Greenberg ME. Activity-dependent transcription and disorders of human cognition. Am J Psychiatry. 2009;166:14-15.
9. Amaral DG,Witter MP. The three-dimensional organization of the hippocampal formation: a review of the anatomical data. Neuroscience. 1989;31:571-591.
10. Tamminga CA, Stan AD, Wagner AD. The hippocampal formation in schizophrenia. Am J Psychiatry. 2010;167:1-16.
11. Tamminga CA. Schizophrenia and glutamatergic transmission. Crit Rev Neurobiol. 1998;12:21-36.
12. Joseph TC. Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol. 2006;V26:363-382.
13. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. 1957. J Neuropsychiatry Clin Neurosci. 2000;12:103-113.
14. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg. 1972;19:421-446.
15. Rempel-Clower NL, Zola SM, Squire LR, Amaral DG. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci. 1996;16:5233-5255.
16. Corkin S. Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H.M. Semin Neurol. 1984;4:249-259.
17. O'Reilly RC, Rudy JW. Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol Rev. 2001;108:311-345.
18. Eichenbaum H. A cortical-hippocampal system for declarative memory. Neuroscience. 2000;1:41-50.
19. Lisman J, Otmakhova N. Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the socratic model to account for normal and aberrant effects of dopamine. Hippocampus. 2001;11:551-568.
20. Schacter DL, Wagner AD. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus. 1999;9:7-24.
21. Cohen N, Eichenbaum H. Memory, Amnesia, and the Hippocampal System. Cambridge, UK: MIT Press; 1993.
22. McClelland JL, McNaughton BL, O'Reilly RC. 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.
23. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans [published erratum appears in Psychol Rev 1992 Jul;99(3):582]. Psychol Rev. 1992;99:195-231.
24. Gabrieli JD. Cognitive neuroscience of human memory. Annu Rev Psychol. 1998;49:87-115.
25. Norman KA, O'Reilly RC. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol Rev. 2003;110:611-646.
26. Preston AR, Wagner AD. The Medial Temporal Lobe and Memory. In: Kesner RP and Martinez J. Neurobiology of Learning and Memory. 2nd ed. New York, NY: Elsevier, Inc.; 2007:305-337.
27. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci. 1993;16:547-563.
28. Lavenex P, Amaral DG. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus. 2000;10: 420-430.
29. Duvernoy H. The Human Hippocampus. New York, NY: Springer; 1998.
30. Insausti R, Juottonen K, Soininen H, et al. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. AJNR Am J Neuroradiol. 1998;19:659-671.
31. Suzuki W, Amaral DG. Perirhinal and parahippocampal cortices of the macaque monkey: cytoarchitectonic and chemoarchitectonic organization. J Comp Neurol. 2003;463:67-91.
32. Lavenex P, Banta LP, Amaral DG. Postnatal development of the primate hippocampal formation. Dev Neurosci. 2007; 29:179-192.
33. O'Reilly RC, McClelland JL. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. 1994;4:661-682.
34. Leutgeb S, Leutgeb JK. Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem. 2007;14:745-757.
35. Bakker A, Kirwan CB, Miller M, Stark CE. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science. 2008;319:1640-1642.
36. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci. 1971;262:23-81.
37. Witter MP, Wouterlood FG, Naber PA, Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci. 2000;9:1-24.
38. Amaral DG, Witter MP. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience. 1989;31:571-591.
39. Lawrence JJ, McBain CJ. Interneuron diversity series: containing the detonation-feedforward inhibition in the CA3 hippocampus. Trends Neurosci. 2003;26:631-640.
40. Toth K, Suares G, Lawrence JJ, Philips-Tansey E, McBain CJ. Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci. 2000;20:8279-8289.
41. Pelkey KA, McBain CJ. Target-cell-dependent plasticity within the mossy fibre-CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites. J Physiol. 2008;586:1495-1502.
42. Katsel P, ByneW, Roussos P, Tan W, Siever L, Haroutunian V. Astrocyte and glutamate markers in the superficial, deep, and white matter layers of the anterior cingulate gyrus in schizophrenia. Neuropsychopharmacology. 2011;36:1171-1177.
43. Izquierdo I, Medina JH. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem. 1997;68:285-316.
44. Biou V, Bhattacharyya S, Malenka RC. Endocytosis and recycling of AMPA receptors lacking GluR2/3. Proc Natl Acad Sci USA. 2008;105:1038-1043.
45. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science. 2006;313:1093-1097.
46. Citri A, Malenka RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology. 2008;33:18-41.
47. Sudhof TC, Malenka RC. Understanding synapses: past, present, and future. Neuron. 2008;60:469-476.
48. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982; 2:32-48.
49. Bear MF. Bidirectional synaptic plasticity: from theory to reality. Philos Trans R Soc Lond B Biol Sci. 2003;358:649-655.
50. Iny K, Heynen AJ, Sklar E, Bear MF. Bidirectional modifications of visual acuity induced by monocular deprivation in juvenile and adult rats. J Neurosci. 2006;26:7368-7374.
51. Lisman J, Raghavachari S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE. 2006;2006:re11.
52. Philpot BD, Cho KK, Bear MF. Obligatory role of NR2A for metaplasticity in visual cortex. Neuron. 2007;53:495-502.
53. Chen WS, Bear MF. Activity-dependent regulation of NR2B translation contributes to metaplasticity in mouse visual cortex. Neuropharmacology. 2007;52:200-214.
54. Kessels HW, Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron. 2009;61:340-350.
55. Abraham WC, Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996;19:126-130.
56. Perez-Otano I, Ehlers MD. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci. 2005;28: 229-238.
57. Ghose S, Chin R, Lewis-Amezcua K, Frost DO, Roberts R, Tamminga C. Distinct gene expression correlations in schizophrenia between NR1 and GAD67 in the anterior hippocampus. 190.23/NN11. Society of Neuroscience Abstract. 2006. http://www.abstractsonline.com/viewer/viewAbstractPrint Friendly.asp?CKey= {F8CCA0FB-FE7B-4A8D-99AD-7F03-C79C2115}&SKey={385A8D36-679C-4381-9CE3- DA1A4B2 76770}&MKey={D1974E76-28AF-4C1C-8AE8-4F73B56247-A7}&AKey= {3A7DC0B9-D787-44AA-BD08-FA7BB2FE-9004}.
58. Gao XM, Sakai K, Roberts RC, Conley RR, Dean B, Tamminga CA. 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.
59. Law AJ, Deakin JF. Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses. Neuroreport. 2001;12:2971-2974.
60. Eastwood SL, McDonald B, Burnet PWJ, Beckwith JP, Kerwin RW, Harrison PJ. Decreased expression of mRNAs encoding non-NMDA glutamate receptors GluR1 and GluR2 in medial temporal lobe neurons in schizophrenia. Mol Brain Res. 1995;29:211-223.
61. Reif A, Fritzen S, Finger M, et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry. 2006;11:514-522.
62. Kolomeets NS, Orlovskaya DD, Uranova NA. Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse. 2007;61:615-621.
63. Porter RH, Eastwood SL, Harrison PJ. Distribution of kainate receptor subunit mRNAs in human hippocampus, neocortex, and cerebellum, and bilateral reduction of hippocampal GluR6 and KA2 transcripts in schizophrenia. Brain Res. 1997;751:217-231.
64. Lauer M, Beckmann H, Senitz D. Increased frequency of dentate granule cells with basal dendrites in the hippocampal formation of schizophrenics. Psychiatry Res. 2003;122:89-97.
65. Kolomeets NS, Orlovskaya DD, Rachmanova VI, Uranova NA. Ultrastructural alterations in hippocampal mossy fiber synapses in schizophrenia: a postmortem morphometric study. Synapse. 2005;57:47-55.
66. Rosoklija G, Toomayan G, Ellis SP, et al. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry. 2000;57:349-356.
67. Schobel SA, Lewandowski NM, Corcoran CM, et al. Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Arch Gen Psychiatry. 2009;66:938-946.
68. Lahti AC, Weiler MA, Holcomb HH, Tamminga CA, Carpenter WT, McMahon R. Correlations between rCBF and symptoms in two independent cohorts of drug-free patients with schizophrenia. Neuropsychopharmacology. 2006;31:221-230.
69. Molina V, Sanz J, Sarramea F, Benito C, Palomo T. Prefrontal atrophy in first episodes of schizophrenia associated with limbic metabolic hyperactivity. J Psychiatr Res. 2005; 39:117-127.
70. Ragland JD, Gur RC, Valdez JN, et al. Levels-of-processing effect on frontotemporal function in schizophrenia during word encoding and recognition. Am J Psychiatry. 2005;162: 1840-1848.
71. Malaspina D, Harkavy-Friedman J, Corcoran C, et al. Resting neural activity distinguishes subgroups of schizophrenia patients. Biol Psychiatry. 2004;56:931-937.
72. Medoff DR, Holcomb HH, Lahti AC, Tamminga CA. Probing the human hippocampus using rCBF: contrasts in schizophrenia. Hippocampus. 2001;11:543-550.
73. Fletcher P. The missing link: a failure of fronto-hippocampal integration in schizophrenia. News Views. 1998;1:266-267.
74. Heckers S, Rauch SL, Goff D, et al. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature. 1998;1:318-323.
75. Nordahl TE, Kusubov N, Carter C, et al. Temporal lobe metabolic differences in medication-free outpatients with schizophrenia via the PET-600. Neuropsychopharmacology. 1996;15:541-554.
76. Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frackowiak RS. Patterns of cerebral blood flow in schizophrenia. Br J Psychiatry. 1992;160:179-186.
77. Tamminga CA, Thaker GK, Buchanan R, et al. Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. Arch Gen Psychiatry. 1992;49:522-530.
78. Gur RE. Left hemisphere dysfunction and left hemisphere overactivation in schizophrenia. J Abnorm Psychol. 1978;87: 226-238.
79. Achim AM, Bertrand MC, Sutton H, et al. Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. Arch Gen Psychiatry. 2007;64:999-1014.
80. Thermenos HW, Seidman LJ, Poldrack RA, et al. Elaborative verbal encoding and altered anterior parahippocampal activation in adolescents and young adults at genetic risk for schizophrenia using FMRI. Biol Psychiatry. 2007;61:564-574.
81. Ongur D, Cullen TJ, Wolf DH, et al. The neural basis of relational memory deficits in schizophrenia. Arch Gen Psychiatry. 2006;63:356-365.
82. Keri S, Nagy O, Kelemen O, Myers CE, Gluck MA. Dissociation between medial temporal lobe and basal ganglia memory systems in schizophrenia. Schizophr Res. 2005;77: 321-328.
83. Holt DJ, Weiss AP, Rauch SL, et al. Sustained activation of the hippocampus in response to fearful faces in schizophrenia. Biol Psychiatry. 2005;57:1011-1019.
84. Heckers S, Zalesak M, Weiss A, Ditman T, Titone D. Hippocampal activation during transitive inference in humans. Hippocampus. 2004;14:153-162.
85. Jessen F, Scheef L, Germeshausen L, et al. Reduced hippocampal activation during encoding and recognition of words in schizophrenia patients. Am J Psychiatry. 2003;160:1305-1312.
86. Leube DT, Rapp A, Buchkremer G, et al. Hippocampal dysfunction during episodic memory encoding in patients with schizophrenia-an fMRI study. Schizophr Res. 2003;64: 83-85.
87. Eyler-Zorrilla LT, Jeste DV, Paulus MP, Brown GG. Functional abnormalities of medial temporal cortex during novel picture learning among patients with chronic schizophrenia. Schizophr Res. 2002;59:187-198.
88. Andreasen NC, O'Leary DS, Flaum M, et al. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naive patients. Lancet. 1997;349:1730-1734.
89. Deicken RF, Pegues M, Amend D. Reduced hippocampal Nacetylaspartate without volume loss in schizophrenia. Schizophr Res. 1999;37:217-223.
90. Stan AD, Ghose S, Gao XM, et al. Human postmortem tissue: what quality markers matter? Brain Res. 2006;1123: 1-11.
91. Mirnics K, Middleton FA, Marquez A, Lewis DA, Levitt P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron. 2000;28:53-67.
92. Eastwood SL, Cairns N, Harrison PJ. Synaptophysin gene expression in schizophrenia. Br J Psychiatry. 2000;176:236-242.
93. Deakin JF, Simpson MDC. A two-process theory of schizophrenia: evidence from studies in post-mortem brain. J Psychiatr Res. 1997;31:277-295.
94. Altar CA, Jurata LW, Charles V, et al. Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry. 2005;58:85-96.
95. Duan X, Chang JH, Ge S, et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell. 2007;130:1146-1158.
96. Lichtenstein P, Yip BH, Bjork C, et al. Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet. 2009;373: 234-239.
97. Li B, Woo RS, Mei L, Malinow R. The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron. 2007;54:583-597.
98. Clelland CD, Choi M, Romberg C, et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science. 2009;325:210-213.
99. Hoffman RE, Grasemann U, Gueorguieva R, Quinlan D, Lane D, Miikkulainen R. Using computational patients to evaluate illness mechanisms in schizophrenia. Biol Psychiatry. 2011;69:997-1005.