Hippocampal afferents to the rat prefrontal cortex: Synaptic targets and relation to dopamine terminals

Journal of Comparative Neurology

Volumn 369, Issue 1, 1996, Pages 1-15

  Carr, David B ^a   Sesack, Susan R ^a  

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

Author keywords

hippocampus; infralimbic cortex; prelimbic cortex; subiculum; ultrastructure

Indexed keywords

ANIMAL TISSUE; ARTICLE; COGNITION; DOPAMINERGIC NERVE CELL; HIPPOCAMPUS; LIMBIC CORTEX; MALE; NERVE PROJECTION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SENSORY NERVE;

AFFERENT PATHWAYS; ANIMALS; DOPAMINE; HIPPOCAMPUS; HORSERADISH PEROXIDASE; IMMUNOENZYME TECHNIQUES; MALE; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NERVE ENDINGS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TYROSINE 3-MONOOXYGENASE;

EID: 0029984555     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960520)369:1<1::AID-CNE1>3.0.CO;2-7     Document Type: Article

References (93)

1. Akil, M., and D.A. Lewis (1993) The dopaminergic innervation of monkey entorhinal cortex. Cerebral Cortex 3:533-550.
2. Asan, E. (1993) Comparative single and double immunolabelling with antisera against catecholaraine biosynthetic enzymes: Criteria for the identification of dopaminergic, noradrenergic and adrenergic structures in selected rat brain areas. Histochemistry 99:427-442.
3. Audinat, E., F. Conde, and F. Crépel (1988) Cortico-cortical connections of the limbic cortex of the rat. Exp. Brain Res. 69:439-443
4. Beaulieu, C., and M. Colonnier (1985) A laminar analysis of the number of round-assymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. J. Comp. Neurol. 231:180-189.
5. Bouyer, J J., D.H. Park, T.H. Joh, and V.M. Pickel (1984) Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res. 302:267-275.
6. Brozoski, T.J., R.M. Brown, H.E. Rosvold, and P S Goldman (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey Science 205:929-932.
7. Carlsson, A. (1988) The current status of the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1:179-186.
8. Carr, D.B , H.C. Wolf, and S.R. Sesack (1994) Hippocampal afferents to the rat prefrontal cortex, synaptic targets and relation to dopamine terminals. Soc. Neurosci. Abstr. 20:530.
9. 3H]GABA. Neuroscience 22:425-439.
10. Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9:268-287.
11. DeFelipe, J , and I. Farinas (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs Prog. Neurobiol. 39:563-607.
12. Dehay, C., R.J. Douglas, K.A.C. Martin, and C. Nelson (1991) Excitation by gemculocortical synapses is not 'vetoed' at the level of dendritic spines in cat visual cortex. J. Physiol. 440:723-734.
13. Descarries, L., B. Lemay, G. Doucet, and B Berger (1987) Regional and laminar density of the dopamine innervation in adult rat cerebral cortex Neuroscience 21:807-824
14. Divac, I., A. Kosmal, A. Björkhmd, and O. Lindvall (1978) Subcortical projections to the prefrontal cortex in the rat as revealed by the horseradish peroxidase technique. Neuroscience 3:785-796.
15. Ferino, F., A.-M. Thierry, and J. Glowinski (1987) Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp. Brain Res 65:421-426.
16. Friedman, H. R , and P.S. Goldman-Rakic (1988) Activation of the hippocampus and dentate gyrus by working-memory: a 2-deoxyglucose study of behaving rhesus monkeys J Neurosci. 8:4693-4706.
17. Fuller, T. A., F.T. Russchen, and J.L. Price (1987) Sources of presumptive glutamatergic/aspartergic afferents to the rat ventral striatopallidal region. J. Comp. Neurol. 258 317-338.
18. Fuster, J.M. (1991) The prefrontal cortex and its relation to behavior. Prog. Brain Res. 87:201-211.
19. Goeders, N.E., and J.E. Smith (1986) Reinforcing properties of cocaine in the medial prefrontal cortex: Primary action on presynaptic dopaminergic terminals. Pharmac. Biochem. Behav 25:191-199.
20. Goeders, N.E., and J.E. Smith (1980) Cortical dopaminergic involvement in cocaine reinforcement. Science 221:773-775.
21. Goldman-Rakic, P.S., C. Leranth, S.M. Williams, N. Mons, and M. Geffard (1989) Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc. Natl. Acad. Sci. 86:9015-9019.
22. Gray, E.G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study. J. Anat 93:420-433.
23. Houser, C.R., J E. Vaughn, S.H C. Hendry, E.G. Jones, and A. Peters (1984) GABA neurons in the cerebral cortex. In E. Jones and A. Peters (eds): Cerebral Cortex. New York: Plenium, pp. 63-89.
24. Hsu, S.-M., L. Raine, and H. Fanger (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques J. Histochem Cytochem. 29:577-580
25. Jay, T. M., A.-M. Thierry, L. Wiklund, and J Glowinski (1992) Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission Eur. J. Neurosci. 4:1285-1295.
26. Jay, T.M., J. Glowinski, and A.-M. Thierry (1989) Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res. 505:337-340.
27. Jay, T.M., and M.P Witter (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-Leucoagglutinin. J. Comp. Neurol. 313:574-586
28. Joh, T., C Gegham, and D. Reis (1973) Immunocytochemical demonstration of increased tyrosine hydroxylase protein in sympathetic ganglia and adrenal medulla elicited by reserpine. Proc. Natl Acad. Sci. U.S.A. 70:2767-2771.
29. Jones, E.G., and T.P.S. Powell (1969) Morphological variations in the dendritic spines of the neocortex. J. Cell Sci. 5.509-529.
30. Koch, C., and T. Poggio (1983a) Electrical properties of dendritic spines. Trends Neurosci. 6.80-83.
31. Koch, C., and T Poggio (1983b) A theoretical analysis of electrical properties of spines. Proc. R. Soc Lond. 218:455-477
32. Kolb, B. (1984) Functions of the frontal cortex of the rat: A comparative review. Brain Res. Rev. 8:65-98.
33. Krettek, J.E., and J. L. Price (1977a) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J. Comp. Neurol. 171:157-192.
34. Krettek, J.E., and J.L. Price (1977b) Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol. 172:687-722.
35. Laroche, S., T.M. Jay, and A.-M. Thierry (1990) Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci. Lett. 114:184-190.
36. LaVail, J.H., and M.M. LaVail (1974) The retrograde intra-axonal transport of horseradish peroxidase in the chick visual system. J. Comp. Neurol 157:303-357.
37. Le Moal, M., and H. Simon (1991) Mesocorticolimbic dopaminergie network: functional and regulatory roles Physiol. Rev. 71:155-234.
38. Lemann, W., C.B. Saper, D.B. Rye, and B.H Wainer (1985) Stabilization of TMB reaction product for electron microscopic retrograde and anterograde fiber tracing. Brain Res. Bull 14:277-281.
39. Leranth, C., and M. Frotscher (1989) Organization of the septal region in the rat brain: Cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J. Comp. Neurol. 289:304-314.
40. Leranth, C., and V.M Pickel (1989) Electron microscopic preembedding double-immunostaining methods. In L Heimer and L Záborszky (eds): Neuroanatomical Tract Tracing Methods 2: Recent Progress. New York: Plenum, pp. 129-172.
41. Lindvall, O , and A Björklund (1984) General organization of cortical monoamine systems. In L. Descarries, T. Reader, and H. Jasper (eds): Monoamine Innervation of the Cerebral Cortex. New York. Alan R. Liss, Inc., pp. 9-40.
42. Mahut, H., S. Zola-Morgan, and M. Moss (1982) Hippocampal resections impair associative learning and recognition memory in the monkey. J. Neurosci. 2:1214-1229.
43. McDonald, A.J (1987) Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: A fluorescence retrograde transport study in the rat. J. Comp. Neurol. 262:46-58.
44. McDonald, A.J. (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1-14.
45. McGuire, B.A., C.D. Gilbert, P.K. Rivlin, and T.N. Wiesel (1991) Targets of horizontal connections in macaque primary visual cortex. J. Comp. Neurol. 305:370-392.
46. Meredith, G E , and F.G. Wouterlood (1990) Hippocampal and midline thalamic fibers and terminals in relation to the choline acetyltransferase-immunoreactive neurons in nucleus accumbens of the rat: a light and electron microscopic study. J Comp. Neurol. 296.204-221.
47. Mesulam, M -M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26:106-117.
48. Mugniani, E., and V.L Friedrich (1981) Electron microscopy: Identification and study of normal and degenerating neural elements by electron microscopy. In L. Heimer and M.J. RoBards (eds) Neuroanatomical Tract-Tracing Methods. New York. Plenum, pp. 377-406.
49. Noack, H.J., and D.A Lewis (1989) Antibodies directed against tyrosine hydroxylase differentially recognize noradrenergic axons in monkey neocortex. Brain Res. 500.313-324.
50. Ordronneau, P., P B.-M. Lindström, and P. Petrusz (1981) Four unlabeled antibody bridge techniques: A comparison. J. Histochem Cytochem. 29:1397-1404
51. Papadopoulos, G C., J.G. Parnavelas, and R.M. Bujis (1989) Light and electron microscopic immunocytochemical analysis of the noradrenaline innervation of the rat visual cortex. J. Neurocytol. 18:1-10
52. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
53. Peters, A , S.L. Palay, and H. Webster (1991) The Fine Structure of the Nervous System: Neurons and Their Supporting Cells. New York: Oxford
54. Pongrácz, F. (1985) The function of dendritic spines: A theoretical study. Neuroscience 15:933-946.
55. Qian, N., and T.J. Sejnowski (1990) When is an inhibitory synapse effective? Proc. Natl. Acad. Sci. 87:8145-8149.
56. Rall W., and I. Segev (1988) Synaptic integration and excitable dendritic spine clusters: Structure/function. In R. Lasek and M. Black (eds): Intrinsic Determinants of Neuronal Form and Function. New York: Liss, pp. 263-282.
57. Rosenkilde, C.E. (1983) Functions of the prefrontal cortex: Behavioral investigations using ablation and electrophysiological techniques in rats, eats, dogs, and monkeys. Acta Physiol. Scand. Suppl 514:4-58.
58. Ruit, K.G., and E.J. Neafsey (1988) Cardiovascular and respiratory responses to electrical and chemical stimulation of the hippocampus in anesthetized and awake rats. Brain Res. 457:310-321.
59. Barter, M., and H J Markowitsch (1983) Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex of the rat. Brain Res. Bull. 10:607-622.
60. Sawaguchi, T., and P.S Goldman-Rakic (1991) D1 dopamine receptors in prefrontal cortex: Involvement in working memory. Science 251:947-950
61. Sawaguchi, T , and P.S Goldman-Rakic (1994) The role of D1-dopamine receptor in working memory: Local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing and oculomotor delayed-response task. J Neurophysiol. 72:515-528.
62. Segev, I., and W Rall (1988) Computational study of an excitable dendritic spine. J. Neurophysiol. 60:499-523
63. Séguéla, P., K.C Watkins, and L. Descarries (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat. Brain Res. 442:11-22.
64. Séguéla, P., K.C Watkins, and L. Descarries (1989) Ultrastructural relationships of serotonin axon terminals in the cerebral cortex of the adult rat J. Comp. Neurol. 289:129-142.
65. Séguéla, P., K.C. Watkins, M. Geffard, and L. Descarries (1990) Noradrenaline axon terminals in adult rat neocortex: An immunocytochemical analysis in serial thin sections Neuroscience 35:249-264.
66. Sesack, S.R., A.Y. Deutch, R.H. Roth, and B S Bunney (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.
67. Sesack, S.R., and V.M. Pickel (1990) In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res 527 266-279.
68. Sesack, S.R., and V.M Pickel (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp. Neurol. 320:145-160.
69. Sesack, S.R., C.L. Snyder, and D.A. Lewis (1995a) Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex, J. Comp. Neurol. 363:264-280.
70. Sesack, S.R., S.W. King, C N Bressler, S.J. Watson, and D.A Lewis (1995b) Electron microscopic visualization of dopamine D2 receptors in the forebrain: Cellular, regional, and species comparisons. Soc. Neurosci. Abstracts 21:365.
71. Shepherd, G.H., and R K. Brayton (1987) Logic operations are properties of computer-simulated interactions between excitable dendritic spines Neuroscience 21:151-165.
72. Simon, H , B. Scatton, and M. Le Moal (1980) Dopaminergic A10 neurones are involved in cognitive functions. Nature 286:150-151.
73. Smiley, J F., and P.S. Goldman-Rakic (1993) Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy a laminar analysis using the silver-enhanced diaminobenzidine Sulfide (SEDS) immunolabelling technique. Cerebral Cortex 3:223-238.
74. Smiley, J.F., A.I. Levey, BJ Ciliax, and P.S. Goldman-Rakic (1994) D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: Predominant and extrasynaptic localization in dendritic spines. Proc. Natl. Acad. Sci. U.S.A. 91:5720-5724.
75. Somogyi, P., and I. Soltész (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19:1051-1065.
76. Steinbusch, H.W.M., and F.J.H. Tilders (1987) Immunohistochemical techniques for light-microscopical localization of dopamine, noradrenaline, serotonin and histamine in the central nervous system. In H.W.M. Steinbusch (ed): Monoaminergic Neurons. Light Microscopy and Ultrastructure. New York: John Wiley & Sons, pp. 125-166.
77. Swanson, L.W., and C. Köhler (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat J Neurosci. 6:3010-3023.
78. Swanson, L.W. (1981) A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 217:150-154
79. Totterdell, S., and A.D. Smith (1989) Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J. Chem. Neuroanat. 2:285-298.
80. Umbriaco, D., K.C. Watkins, L. Descarries, C. Cozzari, and B.K. Hartman (1994) Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: An electron microscopic study in serial sections. J. Comp. Neurol. 348:351-375.
81. Van Eden, C.G., E.M.D Hoorneman, R.M. Buijs, M.A H. Matthijssen, M Geffard, and H B.M Uylings (1987) Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level. Neuroscience 22:849-862.
82. Van Eden, C.G , VA.F. Lamme, and H.B.M. Uylings (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat: A combined retrograde and anterograde tracer study. Eur J. Neurosci. 4:77-97
83. 1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol. 302:515-528.
84. Verney, C., C. Alvarez, M. Geffard, and B Berger (1990) Ultrastructural double-labelling study of dopamine terminals and GABA-containing neurons in rat anteromedial cerebral cortex. Eur. J. Neurosci 2:960-972.
85. Walaas, I., and F. Fonnum (1979) The effects of surgical and chemical lesions on neurotransmitter candidates in the nucleus accumbens of the rat. Neuroscience 4:209-216.
86. Walaas, I., and F Fonnum (1980) Biochemical evidence for glutamate as a transmitter in hippocampal efferents to the basal forebrain and hypothalamus in the rat brain. Neuroscience 5:1691-1698.
87. Watanabe, T , and H. Niki (1985) Hippocampal unit activity and delayed response in the monkey Brain Res. 325:241-254.
88. Weinberger, D.R. (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen. Psychiatr. 44:660-669.
89. Wyss, J.M., L.W. Swanson, and W.M Cowan (1980) The organization of the fimbria, dorsal fornix, and ventral hippocampal commissure in the rat. Anat. Embryol. 158:303-316.
90. Yang, C.R., and G.J. Mogenson (1984) Electrophysiological responses of neurones in the nucleus accumbens to hippocampal stimulation and the attenuation of the excitatory responses by the mesolimbic dopaminergic system. Brain Res 324:69-84.
91. Yang, C.R., and G.J. Mogenson (1986) Dopamine enhances terminal excitability of hippocampal-accumbens neurons via D2 receptor: Role of dopamine in presynaptic inhibition. J. Neurosci. 6:2470-2478.
92. Zaczek, R., J.C. Hedreen, and J.T. Coyle (1979) Evidence for a hippocampal-septal glutamatergic pathway in the rat. Exp. Neurol. 65:145-156.
93. Zola-Morgan, S., and L.R Squire (1986) Memory impairment in monkeys following lesions limited to the hippocampus. Behav. Neurosci. 100:155-160