Long-term effects of amygdala GABA receptor blockade on specific subpopulations of hippocampal interneurons

Hippocampus

Volumn 14, Issue 7, 2004, Pages 876-894

  Berretta, Sabina ^a,b   Lange, Nicholas ^a,b,c   Bhattacharyya, Sujoy ^a   Sebro, Ronnie ^a   Garces, Jessica ^a   Benes, Francine M ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Calbindin; Calretinin; Cholecystokinin; Parvalbumin; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN; CALRETININ; CELL MARKER; CHOLECYSTOKININ; GLUTAMATE DECARBOXYLASE; ISOENZYME; PARVALBUMIN; PICROTOXIN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL DENSITY; CELL SUBPOPULATION; CONTROLLED STUDY; DENTATE GYRUS; DRIVE; GABAERGIC TRANSMISSION; IMMUNOREACTIVITY; INTERNEURON; MALE; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE ENDING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BLOCKING; SCHIZOPHRENIA; STATISTICAL MODEL;

ALGORITHMS; AMYGDALA; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL COUNT; CHOLECYSTOKININ; DENTATE GYRUS; GABA ANTAGONISTS; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; LINEAR MODELS; MALE; PARVALBUMINS; PHENOTYPE; PICROTOXIN; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 6044264432     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20002     Document Type: Article

References (91)

1. Abe K. 2001. Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. Jpn J Pharmacol 86:18-22.
2. Akirav I, Richter-Levin G. 1999. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 19:10530-10535.
3. Amaral DG, Cowan WM. 1980. Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189:573-591.
4. Arnold SE. 1997. The medial temporal lobe in schizophrenia. J Neuropsychiatry Clin Neurosci 9:460-470.
5. Baimbridge KG, Miller JJ. 1982. Immunohistochemical localization of calcium binding protein in the cerebellum, hippocampal formation, and olfactory bulb of the rat. Brain Res 223:229.
6. Baimbridge KG, Miller JJ, Parkes CO. 1982. Calcium-binding protein distribution in the rat brain. Brain Res 239:519-525.
7. Barr WB, Ashtari M, Bilder RM, Degreef G, Lieberman JA. 1997. Brain morphometric comparison of first-episode schizophrenia and temporal lobe epilepsy. Br J Psychiatry 170:515-519.
8. Benes FM. 1993. Neurobiological investigations in cingulate cortex of schizophrenic brain. Schizophr Bull 19:537-549.
9. Benes FM. 2000. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Brain Res Rev 31:251-269.
10. Benes FM, Berretta S. 2000. Amygdalo-entorhinal inputs to the hippocampal formation in relation to schizophrenia. In: The parahippocampal region. Ann NY Acad Sci 911:293-304.
11. Benes FM, Berretta S. 2001. GABAergic interneurons. Implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25:1-27.
12. A receptor binding in the hippocampal formation of schizophrenic brain. Synapse 22:338-349.
13. Benes FM, Wickramasinghe R, Vincent SL, Khan Y, Todtenkopf M. 1997a. Uncoupling of GABA-A and benzodiazepine receptor binding activity in the hippocampal formation of schizophrenic brain. Brain Res 755:121-129.
14. A and benzodiazepine receptor binding activity in the hippocampal formation of schizophrenic brain. Brain Res 755:121-129.
15. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS. 1998a. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressive. Biol Psychiatry 44:88-97.
16. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS. 1998b. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 44:88-97.
17. Benes FM, Todtenkopf MS, Kostoulakos P. 2001. GluR5,6,7 subunit immunoreactivity on apical pyramidal cell dendrites in hippocampus of schizophrenics and manic depressives. Hippocampus 11:482-491.
18. Berretta S, Parthasarathy HP, Graybiel AM. 1997. Local release of GABAergic inhibition in the motor cortex induces immediate-early gene expression in indirect pathway neurons of the striatum. J Neurosci 17:4752-4763.
19. Berretta S, Munno DW, Benes FM. 2001. Amygdalar activation alters the hippocampal GABA system: "partial" modelling for postmortem changes in schizophrenia. J Comp Neurol 431:129-138.
20. Berretta S, Pantazopoulos H, Heckers S, Benes FM, Walsh J. 2003. Decreases in volume and parvalbumin-immunoreactive neurons in the amygdala of schizophrenic and bipolar disorder patients. Schizophr Res 60:68-69.
21. Bogerts B. 1993. Recent advances in the neuropathology of schizophrenia. Schizophr Bull 19:431-445.
22. A-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus 10:305-324.
23. Buzsaki G. 1997. Functions for interneuronal nets in the hippocampus. Can J Physiol Pharmacol 75:508-515.
24. Buzsaki G, Chrobak JJ. 1995. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510.
25. Buzsaki G, Penttonen M, Nadasdy Z, Bragin A. 1996. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc Natl Acad Sci USA 93:9921-9925.
26. Cain DP. 1987. Kindling by repeated intraperitoneal or intracerebral injection of picrotoxin transfers to electrical kindling. Exp Neurol 97:243-254.
27. Chagnac-Amitai Y, Connors BW. 1989. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61:747-758.
28. Chapman J. 1966. The early symptoms of schizophrenia. Br J Psychiatry 112:225-251.
29. Chard PS, Jordan J, Marcuccilli CJ, Miller RJ, Leiden JM, Roos RP, Ghadge GD. 1995. Regulation of excitatory transmission at hippocampal synapses by calbindin D28k. Proc Natl Acad Sci USA 92: 5144-5148.
30. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
31. Cunningham MG, Bhattacharyya S, Benes FM. 2002. Amygdala-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453:116-130.
32. Danober L, Pape HC. 1998. Strychnine-sensitive glycine responses in neurons of the lateral amygdala: an electrophysiological and immunocytochemical characterization. Neuroscience 85:427-441.
33. Fendt M, Schwienbacher I, Koch M. 2000. Amygdaloid N-methyl-D-aspartate and gamma-aminobutyric acid(A) receptors regulate sensorimotor gating in a dopamine-dependent way in rats. Neuroscience 98:55-60.
34. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
35. Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU. 2001. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 21:3697-3703.
36. Gotman J, Levtova V. 1996. Amygdala-hippocampus relationships in temporal lobe seizures: a phase-coherence study. Epilepsy Res 25:51-57.
37. Gulyas AI, Miettinen R, Jacobowitz DM, Freund TF. 1992. Calretinin is present in non-pyramidal cells of the rat hippocampus. I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48:1-27.
38. Gulyas AI, Hajos N, Freund TF. 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
39. Harrison PJ. 1999. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 122:593-624.
40. Heizmann CW. 1992. Calcium-binding proteins: basic concepts and clinical implications. Gen Physiol Biophys 11:411-425.
41. Hill D. 1962. The schizophrenia-like psychoses of epilepsy. Philos Trans R Soc Lond Biol 55:315-316.
42. A antagonists directly into the ventral tegmental area and adjacent regions. Behav Neurosci 111:369-380.
43. Iritani S, Kuroki N, Ikeda K, Kazamatsuri H. 1999. Calbindin immunoreactivity in the hippocampal formation and neocortex of schizophrenics. Prog Neuropsychopharmacol Biol Psychiatry 23:409-421.
44. Johansen FF, Tender N, Zimmer J, Baimbridge KG, Diemer NH. 1990. Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci Lett 120:171-174.
45. Keverne EB. 1999. GABA-ergic neurons and the neurobiology of schizophrenia and other psychoses. Brain Res Bull 48:467-473.
46. Kim JJ, Lee HJ, Han JS, Packard MG. 2001. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21:5222-5228.
47. Kodsi MH, Swerdlow NR. 1995. Prepulse inhibition in the rat is regulated by ventral and caudodorsal striato-pallidal circuitry. Behav Neurosci 109:912-928.
48. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
49. Laezza F, Doherty JJ, Dingledine R. 1999. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 285:1411-1414.
50. Laird N, Lange N, Stram D. 1987. Maximum likelihood computations with repeated measures: application of the EM algorithm. J Am Stat Assoc 82:97-105.
51. Laird N, Ware NM. 1982. Random-effects models for longitudinal data. Biometrics 38:963-974.
52. Lange N, Laird NM. 1989. The effect of covariance structure on variance estimation in balanced growth curve models with random parameters. J Am Stat Assoc 84:241-247.
53. Lange N, Ryan L. 1989. Assessing normality in random effects models. Ann Stat 17:624-642.
54. Lipska BK, Weinberger DR. 2000. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23:223-239.
55. Lipska BK, Swerdlow NR, Geyer MA, Jaskiw GE, Braff DL, Weinberger DR. 1995. Neonatal excitotoxic hippocampal damage in rats causes post-pubertal changes in prepulse inhibition of startle and its disruption by apomorphine. Psychopharmacology (Berl) 122:35-43.
56. Lipska BK, Halim ND, Segal PN, Weinberger DR. 2002. Effects of reversible inactivation of the neonatal ventral hippocampus on behavior in the adult rat. J Neurosci 22:2835-2842.
57. Maccaferri G, McBain CJ. 1996. Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16:5334-5343.
58. Magloczky Z, Freund TF. 1995. Delayed cell death in the contralateral hippocampus following kainate injection into the CA3 subfield. Neuroscience 66:847-860.
59. 28K in cultured hippocampal neurons. Neuron 6:41-51.
60. McCool BA, Botting SK. 2000. Characterization of strychnine-sensitive glycine receptors in acutely isolated adult rat basolateral amygdala neurons. Brain Res 859:341-351.
61. McCool BA, Farroni JS. 2001. Subunit composition of strychnine-sensitive glycine receptors expressed by adult rat basolateral amygdala neurons. Eur J Neurosci 14:1082-1090.
62. McMahon LL, Kauer JA. 1997. Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18:295-305.
63. Miettinen R, Gulyas AI, Baimbridge KG, Jacobowitz DM, Freund TF. 1992. Calretinin is present in non-pyramidal cells of the rat hippocampus. II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48:29-43.
64. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. 1996. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
65. Neyman J, Pearson E. 1928. On the use and interpretation of certain test criteria for the purposes of statistical inference. Biometrika 20:175-240; 263-294.
66. Packard MG, Teather LA. 1998. Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobiol Learn Mem 69:163-203.
67. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. 2nd ed. New York: Academic Press.
68. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A. 1999. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 403: 229-260.
69. Pinheiro JC, Bates DM. 2000. Mixed-effects models in S and S-Plus. New York: Springer.
70. Reynolds GP, Czudek C, Andrews HB. 1990. Deficit and hemispheric asymmetry of GABA uptake sites in the hippocampus in schizophrenia. Biol Psychiatry 27:1038-1044.
71. Rogers JH. 1989. Calcium binding proteins: The search for functions. Nature 339:661-662.
72. Roozendaal B, Nguyen BT, Power AE, McGaugh JL. 1999. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci USA 96:11642-11647.
73. Sachdev P. 1998. Schizophrenia-like psychosis and epilepsy: the status of the association. Am J Psychiatry 155:325-336.
74. A receptors in the rat amygdala. Pharmacol Biochem Behav 52:701-706.
75. Schwarzer C, Sperk G. 1995. Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69:705-709.
76. Sidak Z. 1968. On multivariate normal probabilities of rectangles: their dependence on correlations. Ann Math Stat 39:1425-1434.
77. Sidak Z. 1971. On probabilities of rectangles in multivariate Student distributions: their dependence on correlations. Ann Math Stat 42: 169-175.
78. Simonato M, Bregola G, Beani L, Vezzani A, Sala R, Raiteri M, Bonanno G. 1998. Time- and region-specific variations in somatostatin release following amygdala kindling in the rat. J Neurochem 70:252-259.
79. Simpson MDC, Slater P, Slater JF, Deakin JFW, Royston MC, Skan WJ. 1989. Reduced GABA uptake sites in the temporal lobe in schizophrenia. Neurosci Lett 107:211-215.
80. Sloviter RS, Ali-Akbarian L, Horvath KD, Menkens KA. 2001. Substance P receptor expression by inhibitory interneurons of the rat hippocampus: enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. J Comp Neurol 430:283-305.
81. Stevens JR. 1973. An anatomy of schizophrenia? Arch Gen Psychiatry 29:177-189.
82. Stevens JR. 1999. Epilepsy, schizophrenia, and the extended amygdala. Ann NY Acad Sci 877:548-561.
83. Swanson LW. 1992. Brain maps: structure of the rat brain. Amsterdam: Elsevier.
84. Takahashi M, Shirakawa O, Toyooka K, Kitamura N, Hashimoto T, Maeda K, Koizumi S, Wakabayashi K, Takahashi H, Someya T, Nawa H. 2000. Abnormal expression of brain-derived neurotrophic factor and its receptor in the corticolimbic system of schizophrenic patients. Mol Psychiatry 5:293-300.
85. Tamminga CA. 1998. Schizophrenia and glutamatergic transmission. Crit Rev Neurobiol 12:21-36.
86. Todtenkopf MS, Benes FM. 1998. Distribution of glutamate decarboxylase 65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain. Synapse 29:323-332.
87. Toth K, Freund TF. 1992. Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
88. i changes in the dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 76:2896-2906.
89. Verwer RW, Van Vulpen EH, Van Uum JF. 1996. Postnatal development of amygdaloid projections to the prefrontal cortex in the rat studied with retrograde and anterograde tracers. J Comp Neurol 376:75-96.
90. Zhang LX, Smith MA, Kim SY, Rosen JB, Weiss SR, Post RM. 1996. Changes in cholecystokinin mRNA expression after amygdala kindled seizures: an in situ hybridization study. Brain Res Mol Brain Res 35: 278-284.
91. Zhang ZJ, Reynolds GP. 2002. A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55:1-10.