Synaptic interactions among excitatory afferents to nucleus accumbens neurons: Hippocampal gating of prefrontal cortical input

Journal of Neuroscience

Volumn 15, Issue 5 I, 1995, Pages 3622-3639

  O'Donnell, Patricio ^a,b   Grace, Anthony A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

accumbens; amygdala; electrophysiology; fornix; hippocampus; in vivo; intracellular recordings; prefrontal cortex; schizophrenia; striatum

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FORNIX; CHANNEL GATING; HIPPOCAMPUS; MALE; MEMBRANE POTENTIAL; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA;

EID: 0029014332     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-05-03622.1995     Document Type: Article

References (117)

1. Aldridge JW, Gilman S (1991) The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation. Brain Res 543:123-136.
2. Amzica F, Núñez A, Steriade M (1992) Delta frequency (1-4 Hz) oscillations of perigeniculate thalamic neurons and their modulation by light. Neuroscience 51:285-294.
3. Arnold SE, Hyman BT, Van Hoesen GW, Damasio AR (1991) Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry 48:625-632.
4. Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE (1990) Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 147:1457-1462.
5. Berman KF, Weinberger DR (1991) Prefrontal dopamine and defect symptoms in schizophrenia. In: Negative schizophrenic symptoms: pathophysiology and clinical implications (Greden JF, Tandon R, eds). pp 83-95. Washington, DC: American Psychiatric.
6. Berman KF, Zee RF, Weinberger DR (1986) Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. II. Role of neuroleptic treatment, attention, and mental effort. Arch Gen Psychiatry 43:126-135.
7. Boeijinga PH, Pennartz CMA, Lopes da Silva FH (1990) Paired-pulse facilitation in the nucleus accumbens following stimulation of subicular inputs in the rat. Neuroscience 35:301-311.
8. Boeijinga PH, Mulder AB, Pennartz CMA, Manshanden I, Lopes da Silva FH (1993) Responses of the nucleus accumbens following fornix/fimbria stimulation in the rat. Identification and long-term potentiation of mono- and polysynaptic pathways. Neuroscience 53:1049-1058.
9. Bogerts B, Lieberman JA, Ashtari M, Bilder RM, Degreef G, Lerner G, Johns C, Masiar S (1993) Hippocampus-amygdala volumes and psychopathology in chronic schizophrenia. Biol Psychiatry 33:236-246.
10. Buchsbaum MS, Ingvar DH, Kessler R, Waters RN, Cappelletti J, van Kammen DP, King C, Johnson JL, Manning RG, Flynn RW, Mann LS, Bunney WE, Sokoloff L (1982) Cerebral glucography with positron tomography. Use in normal subjects and in patients with schizophrenia. Arch Gen Psychiatry 39:251-259.
11. Buchsbaum MS, Haier RJ, Potkin SG, Nuechterlein K, Bracha HS, Katz M, Lohr J, Wu J, Lottenberg S, Jerabek PA, Trenary M, Tafalla R, Reynolds C, Bunney WE (1992) Frontostriatal disorder of cerebral metabolism in never-medicated schizophrenics. Arch Gen Psychiatry 49:935-942.
12. Calabresi P, Mercuri NB, Stefani A, Bernardi G (1990) Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis. J Neurophysiol 63:651-662.
13. Calabresi P, Mercuri NB, De Murtas M, Bernardi G (1991) Involvement of GABA systems in feedback regulation of glutamate- and GABA- mediated synaptic potentials in rat neostriatum. J Physiol (Lond) 440:581-599.
14. Callaway CW, Hakan RL, Henriksen SJ (1991) Distribution of amygdala input to the nucleus accumbens septi: an electrophysiological investigation. J Neural Transm [Gen Sect] 83:215-225.
15. Carpenter WT, Buchanan RW (1994) Schizophrenia. New Engl J Med 330:681-690.
16. Chang HT, Kitai ST (1986) Intracellular recordings from rat nucleus accumbens neurons in vitro. Brain Res 366:392-396.
17. Chapman L, Chapman J, Miller G (1964) A theory on verbal behavior in schizophrenia. In: Progress in experimental personality research, Vol I (Maher B, ed), pp 49-77. New York: Academic.
18. Chiodo LA, Bunney BS (1983) Typical and atypical neuroleptics: differential effects of chronic administration on the activity of A9 and AlO midbrain dopaminergic neurons. J Neurosci 3:1607-1619.
19. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17-32.
20. De France JF, Marchand JF, Sikes RW, Chronister RB, Hubbard JI (1985) Characterization of fimbria input to nucleus accumbens. J Neurophysiol 54:1553-1567.
21. de Silva WP, Hemsley DR (1977) The influence of context on language perception in schizophrenia. Br J Soc Clin Psychol 16:337-345.
22. Domesick VB (1981) Further observations on the anatomy of nucleus accumbens and caudatoputamen in the rat: similarities and contrasts. In: The neurobiology of the nucleus accumbens (Chronister RB. DeFrance JF, eds), pp 7-39. Brunswick, ME: Hauer Institute.
23. Eichenbaum H, Wiener SI, Shapiro ML, Cohen NJ (1989) The organization of spatial coding in the hippocampus: a study of neural ensemble activity. J Neurosci 9:2764-2775.
24. Falkai P, Bogerts B (1986) Cell loss in the hippocampus of schizophrenics. Eur Arch Psychiatry Neural Sci 236:154-161.
25. Fey ET (1951) The performance of young schizophrenics and young normals on the Wisconsin Card Sorting Test. J Consult Psychol 15: 311-319.
26. Friston KJ (1992) The dorsolateral prefrontal cortex, schizophrenia and PET. J Neural Transm [Suppl] 37:79-93.
27. Fuller TA, Russchen FT, Price JL (1987) Sources of presumptive glutamatergic/aspartergic afferents to the rat ventral striatopallidal region. J Comp Neurol 258:317-338.
28. Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1-24.
29. Grace AA (1992) The depolarization block hypothesis of neuroleptic action: implications for the etiology and treatment of schizophrenia. J Neural Transm [Suppl] 36:91-131.
30. Grace AA, O'Donnell P (1994) Prefrontal cortical input to nucleus accumbens neurons is differentially modulated by dopaminergic and hippocampal afferents. Dopamine '94, in press.
31. Groenewegen HJ, Becker NEHM, Lohman AHM (1980) Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid. Neuroscience 5:1903-1916.
32. Gur RE, Pearlson GD (1993) Neuroimaging in schizophrenia research. Schizophr Bull 19:337-353.
33. Haber SN, Groenewegen HJ, Grove EA, Nauta WJH (1985) Efferent connections of the ventral pallidum: evidence of a dual striatopallidofugal pathway. J Comp Neurol 235:322-335.
34. Hull CD, Bernardi G, Buchwald NA (1970) Intracellular responses of caudate neurons to brain stem stimulation. Brain Res 22:163-179.
35. Jahnsen H, Llinás R (1984) Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol (Lond) 349:227-247.
36. Jarrard LE (1968) Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol Behav 3:65-70.
37. Johansson O, Hökfelt T (1981) Nucleus accumbens: transmitter histochemistry with special reference to peptide-containing neurons. In: The neurobiology of the nucleus accumbens (Chronister RB, DeFrance JF, eds), pp 147-171. Brunswick, ME: Hauer Institute.
38. Kawasaki Y, Maeda Y, Urata K, Higashima M, Yamaguchi N, Suzuki M, Takashima T, Ide Y (1993) A quantitative magnetic resonance imaging study of patients with schizophrenia. Eur Arch Psychiatry Clin Neurosci 242:268-272.
39. Kelley AE, Domesick VB (1982) The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7:2321-2335.
40. Kerwin R, Patel S, Meldrum B (1990) Quantitative autoradiographic analysis of glutamate binding sites in the hippocampal formation in normal and schizophrenic brain post mortem. Neuroscience 39:25-32.
41. Kesner RP, Bolland BL, Dakis M (1993) Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93:462-470.
42. Kita H, Kitai ST (1990) Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol 298:40-49.
43. Kitai ST, Surmeier DJ (1993) Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons. In: Advances in neurology (Narabayashi H, Nagatsu T, Yanagisawa N, Mizuno Y, eds), pp 40-52. New York: Raven.
44. Kombian SB., Malenka RC (1994) Simultaneous LTP of non-NMDA-and LTD of NMDA-receptor-mediated responses in the nucleus accumbens. Nature 368:242-246.
45. Kovelman JA, Scheibel AB (1984) A neurohistological correlate of schizophrenia. Biol Psychiatry 19:1601-1917.
46. Lavín A, Grace AA (1994) The modulation of dorsal thalamic cell activity by the ventral pallidum: its role in the regulation of thalamocortical activity in the basal ganglia. Synapse 18:104-127.
47. Lavoie AM, Mizumori SJY (1994) Spatial, movement- and reward-sensitive discharge by medial ventral striatum neurons in rats. Brain Res 638:157-168.
48. Leung LS, Yim CYC (1993) Rhythmic delta-frequency activities in the nucleus accumbens of anesthetized freely moving rats. Can J Physiol Pharmacol 71:311-320.
49. Liddle PF, Morris DL (1991) Schizophrenic syndromes and frontal lobe performance. Br J Psychiatry 158:340-345.
50. Liddle PF, Friston KJ, Frith CD, Frachowiak RSJ (1992a) Cerebral blood flow and mental processes in schizophrenia. J R Soc Med 85: 224-227.
51. Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frachowiak RSJ (1992b) Patterns of cerebral blood flow in schizophrenia. Br J Psychiatry 160:179-186.
52. Lipska BK, Jaskiw GE, Weinberger DR (1993) Postpuberal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 9:67-75.
53. Llinás R, Yarom Y (1981) Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol (Lond) 315:549-567.
54. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654-1664.
55. Lopes da Silva FH, Witter MR Boeijinga PH, Lohman AH (1990) Anatomic organization and physiology of the limbic cortex. Physiol Rev 70:453-511.
56. McCormick DA, Pape H-C (1990) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol (Lond) 431:291-318.
57. Meredith GE, Pennartz CMA, Groenewegen HJ (1993) The cellular framework for chemical signalling in the nucleus accumbens. In: Chemical signaling in the basal ganglia (Arbuthnott GW, Emson PC, eds), pp 3-24. Amsterdam: Elsevier.
58. Mittleman G, LeDuc PA, Whishaw IQ (1993) The role of D1 and D2 receptors in the heightened locomotion induced by direct and indirect dopamine agonists in rats with hippocampal damage: an animal analogue of schizophrenia. Behav Brain Res 55:253-267.
59. Mogenson GJ, Yang CR (1991) The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. In: The basal forebrain (Napier TC, ed), pp 267-290. New York: Plenum.
60. Mogenson GM, Yim CC (1991) Neuromodulatory functions of the mesolimbic dopamine system: electrophysiological and behavioral studies. In: The mesolimbic dopamine system: from motivation to action (Willner P, Scheel-Krüger J, eds), pp 105-130. New York: Wiley.
61. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between limbic system and the motor system. Prog Neurobiol 14:69-97.
62. Myles-Worsley M, Johnston WA, Wender PH (1991) Spontaneous selective attention in schizophrenia. Psychiatry Res 39:167-179.
63. Nisenbaum ES, Berger TW (1992) Functionally distinct subpopulations of striatal neurons are differentially regulated by GABAergic and dopaminergic inputs. I. An in vivo analysis. Neuroscience 48:561-578.
64. O'Donnell P, Grace AA (1993a) Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 13:3456-3471.
65. O'Donnell P., Grace AA (1993b) Physiological and morphological properties of accumbens core and shell neurons recorded in vitro. Synapse 13:135-160.
66. 2-mediated attenuation of cortical excitation in nucleus accumbens neurons recorded in vitro. Brain Res 634:105-112.
67. O'Donnell P, Grace AA (1994b) Hippocampal gating of prefrontal cortical input onto nucleus accumbens neurons recorded intracellularly in vivo. Soc Neurosci Abstr 20:566.
68. O'Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419-439.
69. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
70. Onn S-P, Berger TW, Grace AA (1994) Identification and characterization of striatal cell subtypes using in vivo intracellular recording in rats. I. Basic physiology and response to corticostriatal fiber stimulation. Synapse 16:161-180.
71. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Sydney: Academic.
72. Pennartz, CMA, Boeijinga PH, Kitai ST, Lopes da Silva FH (1991) Contribution of NMDA receptors to postsynaptic potentials and paired-pulse facilitation in identified neurons of the rat nucleus accumbens in vitro. Exp Brain Res 86:190-198.
73. Pennartz CMA, Dolleman-van der Weel MJ, Kitai ST, Lopes da Silva FH (1992a) Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens. J Neurophysiol 67:1325-1334.
74. Pennartz CMA, Dolleman-Van der Weel MJ, Lopes da Silva FH (1992b) Differential membrane properties and dopamine effects in the shell and core of the rat nucleus accumbens studied in vitro. Neurosci Lett 136:109-112.
75. Pennartz CMA, Ameerun RF, Groenewegen HJ, Lopes da Silva FH (1993) Synaptic plasticity in an in vitro slice preparation of the rat nucleus accumbens. Eur J Neurosci 5:107-117.
76. Pettegrew JW, Keshavan M, Panchalingbam K, Strychor S, Kaplan DB, Tretta MG, Allen M (1991) Alterations in brain high-energy phosphate and membrane phospholipid metabolism in first-episode, drugnaive schizophrenics. Arch Gen Psychiatry 48:563-568.
77. Raine A, Lencz T, Reynolds GP, Harrison G, Sheard C, Medley I, Reynolds LM, Cooper JE (1992) An evaluation of structural and functional prefrontal deficits in schizophrenia: MRI and neuropsychological measures. Psychiatry Res 45:123-137.
78. Reinstein DK, Hannigan JH, Isaacson RL (1982) Time course of certain behavioral changes after hippocampal damage and their alteration by dopaminergic intervention into nucleus accumbens. Pharmacol Biochem Behav 17:193-202.
79. Robbins TW (1990) The case for frontostriatal dysfunction in schizophrenia. Schizophr Bull 16:391-402.
80. Seeman P (1987) Dopamine receptors and the dopamine hypothesis of schizophrenia. Synapse 1:133-152.
81. Segal M, Bloom FE (1976) The action of norepinephrine in the rat hippocampus. III. Hippocampal cellular responses to locus coeruleus stimulation in the awake rat. Brain Res 107:499-511.
82. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242.
83. Shapiro RM (1993) Regional neuropathology in schizophrenia: where are we? Where are we going? Schizophr Res 10:187-239.
84. Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Matcalf D, Coleman M, McCarley RW (1992) Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. New Engl J Med 327:604-612.
85. Sherman AD, Davidson AT, Baruah S, Hegwood TS, Waziri R (1991) Evidence of glutamatergic deficiency in schizophrenia. Neurosci Lett 121:77-80.
86. Snyder SH (1973) Amphetamine psychosis: a model of schizophrenia mediated by catecholamines. Am J Psychiatry 130:61-67.
87. Stafstrom CE, Schwindt PC, Flatman JA, Crill WE (1984) Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol 52: 244-263.
88. Steriade M, Llinás RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649-742.
89. Steriade M, Nuñez A, Amzica F (1993) A novel slow (<1 Hz) oscillation of neocortical neuron in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:32552-3265.
90. Su H-S, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582-593.
91. Suddath RL, Christison GW, Torrey EF, Casanova MF, Weinberger DR (1990) Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. New Engl J Med 322:789-794.
92. Sugimori M, Preston RJ, Kitai ST (1978) Response properties and electrical constants of caudate neurons in the cat. J Neurophysiol 41: 1662-1675.
93. Swanson LW, Cowan WM (1975) A note on the connections and development of the nucleus accumbens. Brain Res 92:324-330.
94. Tamminga CA, Thaker GK, Buchanan R, Kirkpatrick B, Alphs LD, Chase TN, Carpenter WT (1992) Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. Arch Gen Psychiatry 49:522-530.
95. Uchimura N, North RA (1991) Baclofen and adenosine inhibit synaptic potentials mediated by gamma-aminobutyric acid and glutamate release in rat nucleus accumbens. J Pharmacol Exp Ther 258:663-668.
96. Uchimura N, Higashi H, Nishi S (1986) Hyperpolarizing and depolarizing actions of dopamine via D-1 and D-2 receptors on nucleus accumbens neurons. Brain Res 375:368-372.
97. Uchimura N, Cherubini E, North RA (1989a) Inward rectification in rat nucleus accumbens neurons. J Neurophysiol 62:1280-1286.
98. Uchimura N, Higashi H, Nishi S (1989b) Membrane properties and synaptic responses of the guinea pig nucleus accumbens neurons in vitro. J Neurophysiol 61:769-779.
99. Ułas J, Cotman CW (1993) Excitatory amino acid receptors in schizophrenia. Schizophr Bull 19:105-117.
100. Waddington JL (1993) Schizophrenia: developmental neuroscience and pathobiology. Lancet 341:531-536.
101. Weinberger DR (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44:660-669.
102. Weinberger DR, Berman KF, Suddath R, Torrey EF (1992) Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am J Psychiatry 149:890-897.
103. White FJ, Wang RY (1983) Differential effects of classical and atypical antipsychotic drugs on A9 and A10 dopamine neurons. Science 221: 1054-1057.
104. White TD, Tan AM, Finch DM (1990) Functional reciprocal connections of the rat entorhinal cortex and subicular complex with the medial frontal cortex: an in vivo intracellular study. Brain Res 533: 95-106.
105. Wilson CJ (1992a) Dendritic morphology, inward rectification, and the functional properties of neostriatal neurons. In: Neural nets: foundations to applications. Single neuron computation (McKenna T, Davis J, Zornetzer SF, eds), pp 141-171. San Diego: Academic.
106. Wilson CJ (1992b) Voltage-gated currents contribute to spontaneous membrane potential shifts in neostriatal projection neurons. Soc Neurosci Abstr 18:849.
107. Wilson CJ (1993) The generation of natural firing patterns in neostriatal neurons. In: Chemical signaling in the basal ganglia (Arbuthnott GW, Emson PC, eds), pp 277-297. Amsterdam: Elsevier.
108. Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220:67-80.
109. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
110. Yang CR, Mogenson GJ (1984) Electrophysiological responses of neurones in the accumbens nucleus to hippocampal stimulation and the attenuation of the excitatory responses by the mesolimbic dopaminergic system. Brain Res 324:69-84.
111. Yang CR, Mogenson GJ (1986) Dopamine enhances terminal excitability of hippocampal-accumbens neurons via D2 receptor: role of dopamine in presynaptic inhibition. J Neurosci 6:2470-2478.
112. 2 receptors in the nucleus accumbens: an electrophysiological and behavioral study. Neuroscience 23:1041-1055.
113. Yim CY, Mogenson GJ (1982) Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine. Brain Res 239:401-415.
114. Yim CY, Mogenson GJ (1986) Mesolimbic dopamine projection modulates amygdala-evoked EPSP in nucleus accumbens neurons: an in vivo study. Brain Res 369:347-352.
115. Yim CY, Mogenson GJ (1988) Neuromodulatory action of dopamine in the nucleus accumbens: an in vivo intracellular study. Neuroscience 26:403-415.
116. Yim CY, Mogenson GJ (1989) Low doses of accumbens dopamine modulate amygdala suppression of spontaneous exploratory activity in rats. Brain Res 477:202-210.
117. Young WS, Alheid GF, Heimer L (1984) The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J Neurosci 4:1626-1638.