Quantification of morphological differences in boutons from different afferent populations to the nucleus accumbens

Brain Research

Volumn 1007, Issue 1-2, 2004, Pages 167-177

  French, Sarah Jane ^a   Totterdell, Susan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Basolateral amygdala; Central medial thalamus; Comparative neuroanatomy; Electron microscopy; Other systems of the CNS; Prefrontal cortex; Ventral subiculum

Indexed keywords

DEXTRAN; GLUTAMINE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL VACUOLE; COMPARATIVE ANATOMY; DENDRITE; ELECTRON MICROSCOPY; HIPPOCAMPUS; MALE; MORPHOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; POSTSYNAPTIC MEMBRANE; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SENSORY NERVE; SUBICULUM; SYNAPSE; THALAMUS;

ANALYSIS OF VARIANCE; ANIMALS; BIOTIN; CELL SIZE; DEXTRANS; MALE; MICROSCOPY, ELECTRON; MITOCHONDRIA; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; STAINING AND LABELING;

EID: 1942535048     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.02.018     Document Type: Article

References (84)

1. Andersen P., Eccles J.C. Locating and identifying postsynaptic inhibitory synapses by the correlation of physiological and histological data. Symp. Biol. Hung. 5:1965;219-242.
2. Andersen P., Eccles J.C., Voorhoeve P.E. Inhibitory synapses on soma of Purkinje cells in the cerebellum. Nature. 199:1963;655-656.
3. Bekkers J.M., Richerson G.B., Stevens C.F. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc. Natl. Acad. Sci. U. S. A. 87:1990;5359-5362.
4. Bennett B.D., Bolam J.P. Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat. Neuroscience. 62:1994;707-719.
5. Berendse H.W., Groenewegen H.J. Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol. 299:1990;187-228.
6. Berendse H.W., Groenewegen H.J. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience. 42:1991;73-102.
7. Berendse H.W., Galis-de Graaf Y., Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 316:1992;314-347.
8. Bolam J.P. Synapses of identified neurons in the neostriatum. Ciba Found. Symp. 107:1984;30-47.
9. Bolam J.P., Somogyi P., Totterdell S., Smith A.D. A second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience. 6:1981;2141-2157.
10. Brog J.S., Salyapongse A., Deutch A.Y., Zahm D.S. The patterns of afferent innervation of the core and shell in the accumbens; part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J. Comp. Neurol. 338:1993;255-278.
11. Canteras N.S., Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 324:1992;180-194.
12. Christie M.J., James L.B., Beart P.M. An excitant amino acid projection from the medial prefrontal cortex to the anterior part of nucleus accumbens in the rat. J. Neurochem. 45:1985;477-482.
13. Cohen R.S., Siekevitz P. Form of the postsynaptic density. A serial section study. J. Cell Biol. 78:1978;36-46.
14. Colonnier M. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9:1968;268-287.
15. Coolen L.M., Jansen H.T., Goodman R.L., Wood R.I., Lehman M.N. A new method for simultaneous demonstration of anterograde and retrograde connections in the brain: co-injections of biotinylated dextran amine and the beta subunit of cholera toxin. J. Neurosci. Methods. 91:1999;1-8.
16. Corvaja N., Doucet G., Bolam J.P. Ultrastructure and synaptic targets of the raphe-nigral projection in the rat. Neuroscience. 55:1993;417-427.
17. Dallvechia-Adams S., Smith Y., Kuhar M.J. CART peptide-immunoreactive projection from the nucleus accumbens targets substantia nigra pars reticulata neurons in the rat. J. Comp. Neurol. 434:2001;29-39.
18. DeFrance J.F., Marchand J.F., Sikes R.W., Chronister R.B., Hubbard J.I. Characterization of fimbria input to nucleus accumbens. J. Neurophysiol. 54:1985;1553-1567.
19. Eccles J.C. The Physiology of Synapses. 1964;Springer-Verlag, Berlin.
20. Finch D.M. Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus. 6:1996;495-512.
21. Finnegan J.M., Pihel K., Cahill P.S., Huang L., Zerby S.E., Ewing A.G., Kennedy R.T., Wightman R.M. Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J. Neurochem. 66:1996;1914-1923.
22. French S.J., Totterdell S. Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens. J. Comp. Neurol. 446:2002;151-165.
23. French S.J., Totterdell S. Individual nucleus accumbens projection neurons receive both basolateral amygdala and ventral subicular afferents. Neuroscience. 119:2003;19-31.
24. French S.J., Hailstone J.C., Totterdell S. Basolateral amygdala efferents to the ventral subiculum preferentially innervate pyramidal cell dendritic spines. Brain Res. 981:2003;160-167.
25. Glavinovic M.I., Vitale M.L., Trifaro J.M. Comparison of vesicular volume and quantal size in bovine chromaffin cells. Neuroscience. 85:1998;957-968.
26. Gray E.G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J. Anat. 93:1959;420-433.
27. Groenewegen H.J., Russchen F.T. Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic, and mesencephalic structures: a tracing and immunohistochemical study in the cat. J. Comp. Neurol. 223:1984;347-367.
28. Groenewegen H.J., Vermeulen-Van der Zee E., te Kortschot A., Witter M.P. Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience. 23:1987;103-120.
29. Groenewegen H.J., Berendse H.W., Meredith G.E., Haber S.N., Voorn P., Wolters J.G., Lohman A.H.M. Functional anatomy of the ventral, limbic system-innervated striatum. Willner P., Scheel-Kruger J. The Mesolimbic Dopamine System: From Motivation to Action. 1991;19-60 Wiley, Chichester.
30. Groenewegen H.J., Wright C.I., Beijer A.V. The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog. Brain Res. 107:1996;485-511.
31. Groenewegen H.J., Wright C.I., Uylings H.B. The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J. Psychopharmacol. 11:1997;99-106.
32. Groenewegen H.J., Galis-de Graaf Y., Smeets W.J. Integration and segregation of limbic cortico-striatal loops at the thalamic level: an experimental tracing study in rats. J. Chem. Neuroanat. 16:1999;167-185.
33. Groenewegen H.J., Mulder A.B., Beijer V.J., Wright C.I., Lopes da Silva F.H., Pennartz C.M.A. Hippocampal and amygdala interactions in the nucleus accumbens. Psychobiology. 27:1999;149-164.
34. Heimer L., Zahm D.S., Churchill L., Kalivas P.W., Wohltmann C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience. 41:1991;89-125.
35. Hussain Z., Johnson L.R., Totterdell S. A light and electron microscopic study of NADPH-diaphorase-, calretinin- and parvalbumin-containing neurons in the rat nucleus accumbens. J. Chem. Neuroanat. 10:1996;19-39.
36. Johnson L.R., Aylward R.L., Hussain Z., Totterdell S. Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience. 61:1994;851-865.
37. Kachidian P., Vuillet J., Nieoullon A., Lafaille G., Kerkerian-Le Goff L. Striatal neuropeptide Y neurones are not a target for thalamic afferent fibres. Neuroreport. 7:1996;1665-1669.
38. Karunanithi S., Marin L., Wong K., Atwood H.L. Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J. Neurosci. 22:2002;10267-10276.
39. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. TINS. 18:1995;527-535.
40. Kelley A.E., Domesick V.B. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience. 7:1982;2321-2335.
41. Kita H., Kitai S.T. Amygdaloid projections to the frontal cortex and the striatum in the rat. J. Comp. Neurol. 298:1990;40-49.
42. Klein R.L., Wilson S.P., Dzielak D.J., Yang W.H., Viveros O.H. Opioid peptides and noradrenaline co-exist in large dense-cored vesicles from sympathetic nerve. Neuroscience. 7:1982;2255-2261.
43. Kowall N.W., Ferrante R.J., Beal M.F., Richardson E.P. Jr., Sofroniew M.V., Cuello A.C., Martin J.B. Neuropeptide Y, somatostatin, and reduced nicotinamide adenine dinucleotide phosphate diaphorase in the human striatum: a combined immunocytochemical and enzyme histochemical study. Neuroscience. 20:1987;817-828.
44. Krettek J.E., Price J.L. Projections from the amygdala to the perirhinal and entorhinal cortices and the subiculum. Brain Res. 71:1974;150-154.
45. Krettek J.E., Price J.L. Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol. 172:1977;687-722.
46. Lapper S.R., Bolam J.P. Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience. 51:1992;533-545.
47. Lapper S.R., Smith Y., Sadikot A.F., Parent A., Bolam J.P. Cortical input to parvalbumin-immunoreactive neurones in the putamen of the squirrel monkey. Brain Res. 580:1992;215-224.
48. McDonald A.J. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience. 44:1991;15-33.
49. Meredith G.E. The synaptic framework for chemical signaling in nucleus accumbens. Ann. N.Y. Acad. Sci. 877:1999;140-156.
50. Meredith G.E., Totterdell S. Microcircuits in nucleus accumben's shell and core involved in cognition and reward. Psychobiology. 27:1999;165-186.
51. Meredith G.E., Wouterlood F.G. 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. 296:1990;204-221.
52. Meredith G.E., Wouterlood F.G., Pattiselanno A. Hippocampal fibers make synaptic contacts with glutamate decarboxylase-immunoreactive neurons in the rat nucleus accumbens. Brain Res. 513:1990;329-334.
53. Meredith G.E., Agolia R., Arts M.P., Groenewegen H.J., Zahm D.S. Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience. 50:1992;149-162.
54. Milhaud M., Pappas G.D. Postsynaptic bodies in the habenula and interpeduncular nuclei of the cat. J. Cell Biol. 30:1966;437-441.
55. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14:1980;69-97.
56. Otake K., Nakamura Y. Single midline thalamic neurons projecting to both the ventral striatum and the prefrontal cortex in the rat. Neuroscience. 86:1998;635-649.
57. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1986;Academic Press, Sydney.
58. Pennartz C.M., Groenewegen H.J., Lopes da Silva F.H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol. 42:1994;719-761.
59. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z. Zellforsch. Mikrosk. Anat. 100:1969;487-506.
60. Petrovich G.D., Risold P.Y., Swanson L.W. Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 374:1996;387-420.
61. Pickel V.M., Reis D.J., Leeman S.E. Ultrastructural localization of substance P in neurons of rat spinal cord. Brain Res. 122:1977;534-540.
62. Pikkarainen M., Ronkko S., Savander V., Insausti R., Pitkanen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 403:1999;229-260.
63. Reiner A., Veenman C.L., Medina L., Jiao Y., Del Mar N., Honig M.G. Pathway tracing using biotinylated dextran amines. J. Neurosci. Methods. 103:2000;23-37.
64. Reynolds E.S. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17:1963;208-212.
65. Rudkin T.M., Sadikot A.F. Thalamic input to parvalbumin-immunoreactive GABAergic interneurons: organization in normal striatum and effect of neonatal decortication. Neuroscience. 88:1999;1165-1175.
66. Sadikot A.F., Rudkin T.M., Smith Y. The amygdalostriatal projection. An analysis of synaptic inputs to GABAergic interneuron subtypes. Ohye C. The Basal Ganglia. vol. V:1996;33-42 Plenum, New York.
67. Sesack S.R., Pickel V.M. In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res. 527:1990;266-279.
68. Sesack S.R., Pickel V.M. 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. 320:1992;145-160.
69. Shinonaga Y., Takada M., Mizuno N. Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience. 58:1994;389-397.
70. Smith A.D., Bolam J.P. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. TINS. 13:1990;259-265.
71. Su H.S., Bentivoglio M. Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J. Comp. Neurol. 297:1990;582-593.
72. Totterdell S., Smith A.D. Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J. Chem. Neuroanat. 2:1989;285-298.
73. Totterdell S., Ingham C.A., Bolam J.P. Immunocytochemistry: I. Pre-embedding staining. Bolam J.P. Experimental Neuroanatomy: A Practical Approach. 1992;103-128 IRL Press, Oxford.
74. Uchizono K. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature. 207:1965;642-643.
75. Uchizono K. Axon identification in the cerebellar cortex of the cat. Arch. Histol. Jpn. 29:1968;399-424.
76. Usuda I., Tanaka K., Chiba T. Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res. 797:1998;73-93.
77. Van der Kloot W., Molgo J., Cameron R., Colasante C. Vesicle size and transmitter release at the frog neuromuscular junction when quantal acetylcholine content is increased or decreased. J. Physiol. 541:2002;385-393.
78. Van der Werf Y.D., Witter M.P., Groenewegen H.J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39:2002;107-140.
79. Wright C.I., Groenewegen H.J. Patterns of convergence and segregation in the medial nucleus accumbens of the rat: relationships of prefrontal cortical, midline thalamic, and basal amygdaloid afferents. J. Comp. Neurol. 361:1995;383-403.
80. Wright C.I., Groenewegen H.J. Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat. Neuroscience. 73:1996;359-373.
81. Wright C.I., Beijer A.V., Groenewegen H.J. Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J. Neurosci. 16:1996;1877-1893.
82. Zahm D.S., Heimer L. Two transpallidal pathways originating in the rat nucleus accumbens. J. Comp. Neurol. 302:1990;437-446.
83. Zahm D.S., Heimer L. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J. Comp. Neurol. 327:1993;220-232.
84. Zahm D.S., Williams E., Wohltmann C. Ventral striatopallidothalamic projection: IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. J. Comp. Neurol. 364:1996;340-362.