Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala

Journal of Comparative Neurology

Volumn 505, Issue 3, 2007, Pages 314-335

  Muller, Jay F ^a   Mascagni, Franco ^a   McDonald, Alexander J ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Electron microscopy; Immunocytochemistry; Monoamines, neuropeptides, calcium binding proteins, calcium calmodulin dependent protein kinase II

Indexed keywords

CALBINDIN; CALRETININ; CHOLECYSTOKININ; PARVALBUMIN; SEROTONIN; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INNERVATION; INTERNEURON; MALE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEROTONINERGIC NERVE CELL; SYNAPSE;

AMYGDALA; ANIMALS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; PARVALBUMINS; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; VASOACTIVE INTESTINAL PEPTIDE;

EID: 36249012512     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21486     Document Type: Article

References (117)

1. Abrams JK, Johnson PL, Hay-Schmidt A, Mikkelsen JD, Shekhar A, Lowry CA. 2005. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133:983-997.
2. Acsady L, Halasy K, Freund TF. 1993. Calretinin is present in non-pyramidal cells of the rat hippocampus-III. Their inputs from the median raphe and medial septal nuclei. Neuroscience 52:829-841.
3. Aggleton JP (ed.). 1992. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss.
4. Aggleton JP. 2000. The amygdala: a functional analysis. New York: Wiley-Liss.
5. Aghajanian, GK. 1995. Electrophysiology of serotonin receptor subtypes and signal transduction pathways. In: Bloom FE, Kupfer DJ, editors. Psychopharmacology: the fourth generation of progress. New York: Raven Press. p 451-460.
6. Bauman MD, Amaral DG. 2005. The distribution of serotonergic fibers in the macaque monkey amygdala: an immunohistochemical study using antisera to 5-hydroxytryptamine. Neuroscience 136:193-203.
7. Beaudet A, Descarries L. 1987. Ultrastructural identification of serotonin neurons. In: Steinbusch HWN, editor. Monoaminergic neurons: light microscopy and ultrastructure. New York: John Wiley & Sons. p 265-313.
8. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. 2001. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8:229-2242.
9. Brinley-Reed M, Mascagni F, McDonald AJ. 1995. Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci Lett 202:45-48.
10. Bruns D, Jahn R. 1995. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377:62-65.
11. Buchan AM, Sikora LK, Levy JG, McIntosh CH, Dyck I, Brown JC. 1985. An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83:175-180.
12. Bunin MA, Wightman RM. 1999. Paracrine neurotransmission in the CNS: involvement of 5-HT. Trends Neurosci 22:377-382.
13. Burghardt NS, Farb CR, Sullivan GM, LeDoux JE. 2000. Immunocytochemical localization of serotonin 1A, 2A, 2C, 3, and 7 receptor subtypes in the lateral amygdala (LA) of the rat. Program No. 465.10. Abstract viewer/Itinerary Planner. Washington DC: Society for Neuroscience.
14. Burghardt NS, Sullivan GM, McEwen BS, Gorman JM, LeDoux JE. 2004. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiatry 55:1171-1178.
15. Canli T, Congdon E, Gutknecht L, Constable RT, Lesch KP. 2005. Amygdala responsiveness is modulated by tryptophan hydroxylase-2 gene variation. J Neural Transm 112:1479-1485.
16. Carlsen J, Heimer L. 1988. The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377-380.
17. Chen A, Hough CJ, Li H. 2003. Serotonin type II receptor activation facilitates synaptic plasticity via N-methyl-D-aspartate-mediated mechanism in the rat basolateral amygdala. Neuroscience 119:53-63.
18. 1A receptors. Eur J Neurosci 10:2163-2172.
19. Conde F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA. 1994. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95-116.
20. DeFelipe J, Jones EG. 1988. A light and electron microscopic study of serotonin-immunoreactive fibers and terminals in the monkey sensory-motor cortex. Exp Brain Res 71:171-182.
21. de Lima AD, Bloom FE, Morrison JH. 1988. Synaptic organization of serotonin-immunoreactive fibers in primary visual cortex of the macaque monkey. J Comp Neurol 274:280-294.
22. de Mello Cruz AP, Pinheiro G, Alves SH, Ferreira G, Mendes M, Faria L, Macedo CE, Motta V, Landeira-Fernandez J. 2005. Behavioral effects of systemically administered MK-212 are prevented by ritanserin microinfusion into the basolateral amygdala of rats exposed to the elevated plus-maze. Psychopharmacology (Berl) 182:345-354.
23. De-Miguel FF, Trueta C. 2005. Synaptic and extrasynaptic secretion of serotonin. Cell Mol Neurobiol 25:297-312.
24. Descarries L, Audet MA, Doucet G, Garcia S, Oleskevich S, Seguela P, Soghomonian JJ, Watkins KC. 1990. Morphology of central serotonin neurons. Brief review of quantified aspects of their distribution and ultrastructural relationships. Ann N Y Acad Sci 600:81-92.
25. Drevets WC. 2003. Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 985:420-444.
26. Drevets WC, Bogers W, Raichle ME. 2002. Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur Neuropsychopharmacol 12:527-544.
27. Erondu NE, Kennedy MB. 1985. Regional distribution of type II Ca2+/ calmodulin-dependent protein kinase in rat brain. J Neurosci 5:3270-3277.
28. Fallon JH, Ciofi P. 1992. Distribution of monoamines within the amygdala. In: Aggleton JP, editor: The amygdala. New York: Wiley-Liss. p 97-114.
29. Farb CR, LeDoux JE. 1999. Afferents from rat temporal cortex synapse on lateral amygdala neurons that express NMDA and AMPA receptors. Synapse 33:218-229.
30. Freund TF, Buzsáki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
31. Freund TF, Gulyas AI, Acsady L, Gores T, Toth K. 1990. Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci U S A 87:8501-8505.
32. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF. 1996. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129-141.
33. Gulyas AI, Acsady L, Freund TF. 1999. Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus. Neurochem Int 34:359-372.
34. Halasy K, Miettinen R, Szabat E, Freund TF. 1992. GABAergic interneurons are the major postsynaptic targets of median raphe afferents in the rat dentate gyrus. Eur J Neurosci 4:144-153.
35. Hall E. 1972. The amygdala of the cat: a Golgi study. Z Zellforsch 134:439-458.
36. Hancock MB. 1986. Two color immunoperoxidase staining: visualization of anatomic relationships between immunoreactive neural elements. Am J Anat 175:343-352.
37. Hariri AR, Holmes A. 2006. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn Sci 10:182-191.
38. Huang YY, Kandel ER. 2007. 5-Hydroxytryptamine induces a protein kinase A/mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J Neurosci 27:3111-3119.
39. Inoue T, Li XB, Abekawa T, Kitaichi Y, Izumi T, Nakagawa S, Koyama T. 2004. Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 497:311-316.
40. Izumi T, Inoue T, Kitaichi Y, Nakagawa S, Koyama T. 2006. Target brain sites of the anxiolytic effect of citalopram, a selective serotonin reuptake inhibitor. Eur J Pharmacol 534:129-132.
41. Jacobowitz DM, Winsky L. 1991. Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304:198-218.
42. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
43. Kawahara H, Yoshida M, Yokoo H, Nishi M, Tanaka M. 1993. Psychological stress increases serotonin release in the rat amygdala and prefrontal cortex assessed by in vivo microdialysis. Neurosci Lett 162:81-84.
44. 28k immunoreactivity in the rat amygdaloid complex and colocalization with gamma-aminobutyric acid. J Comp Neurol 426: 441-467.
45. Koyama S, Kubo C, Rhee JS, Akaike N. 1999. Presynaptic serotonergic inhibition of GABAergic synaptic transmission in mechanically dissociated rat basolateral amygdala neurons. J Physiol 518:525-538.
46. Lamprecht R, LeDoux J. 2004. Structural plasticity and memory. Nat Rev Neurosci 5:45-54.
47. Lanciego JL, Goede PH, Witter MP, Wouterlood FG. 1997. Use of peroxidase substrate Vector VIP for multiple staining in light microscopy. J Neurosci Methods 74:1-7.
48. LeDoux JE, Farb CR, Milner TA. 1991. Ultrastructure and synaptic associations of auditory thalamo-amygdala projections in the rat. Exp Brain Res 85:577-586.
49. 1A receptors in the hippocampus and amygdala. Eur J Pharmacol 532:74-80.
50. 1A receptors. Eur J Neurosci 11:1491-1500.
51. Mascagni F, McDonald AJ. 2003. Immunohistochemical characterization of cholecystokinin containing neurons in the rat basolateral amygdala. Brain Res 976:171-184.
52. 3A receptor imunoreactive interneurons in the rat basolateral amygdala. Neurosci 144:1015-1024.
53. McDonald AJ. 1982. Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat. J Comp Neurol 212:293-312.
54. McDonald AJ. 1992a. Cell types and intrinsic connections of the amygdala. In: Aggleton JP, editor. The amygdala. New York: Wiley-Liss. p 67-96.
55. McDonald AJ. 1992b. Projection neurons of the basolateral amygdala: a correlative Golgi and retrograde tract tracing study. Brain Res Bull 28:179-185.
56. McDonald AJ, Betette R. 2001. Parvalbumin containing neurons in the rat basolateral amygdala: morphology and colocalization of calbindin D-28k. Neuroscience 102:413-425.
57. McDonald AJ, Mascagni F. 2001a. Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681-693.
58. McDonald AJ, Mascagni F. 2001b. Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience 107:641-652.
59. McDonald AJ, Mascagni F. 2002. Immunohistochemical characterization of somatostatin containing interneurons in the rat basolateral amygdala. Brain Res 943:237-244.
60. McDonald AJ, Mascagni F. 2007. Neuronal localization of 5-HT type receptor immunoreactivity in the rat basolateral amygdala. Neuroscience 146:306-320.
61. McDonald AJ, Muller JF, Mascagni F. 2002. GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala. J Comp Neurol 446:199-218.
62. Miettinen R, Freund TF. 1992. Neuropeptide Y-containing interneurons in the hippocampus receive synaptic input from median raphe and GABAergic septal afferents. Neuropeptides 22:185-193.
63. Molliver ME. 1987. Serotonergic neuronal systems: what their anatomic organization tells us about function. J Clin Psychopharmacol. 7:3S-23S.
64. Moore RY, Halaris AE, Jones BE. 1978. Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180:417-438.
65. Morales M, Bloom FE. 1997. The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157-3167.
66. Muller JF, Mascagni F, McDonald AJ. 2003. Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217-236.
67. Muller JF, Mascagni F, McDonald AJ. 2005. Coupled networks of parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Neurosci 25:7366-7376
68. Muller JF, Mascagni F, McDonald AJ. 2006. Pyramidal cells of the rat basolateral amygdala: synaptology and innervation by parvalbumin-immunoreactive interneurons. J Comp Neurol 494:635-650.
69. Muller JF, Mascagni F, McDonald AJ. 2007. Postsynaptic targets of somatostatin-containing interneurons in the rat basolateral amygdala. J Comp Neurol 500:513-519.
70. Oleskevich S, Descarries L, Watkins KC, Seguela P, Daszuta A. 1991. Ultrastructural features of the serotonin innervation in adult rat hippocampus: an immunocytochemical description in single and serial thin sections. Neuroscience 42:777-791.
71. Ottersen OP. 1981. Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J Comp Neurol 202:335-356.
72. Papadopoulos GC, Parnavelas JG, Buijs RM. 1987. Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex. J Neurocytol 16:883-892.
73. Papp EC, Hajos N, Acsady L, Freund TF. 1999. Medial septal and median raphe innervation of vasoactive intestinal polypeptide-containing interneurons in the hippocampus. Neuroscience 90:369-382.
74. Paré D, Smith Y, Paré JF. 1995. Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level. Neuroscience 69:567-583.
75. Paré D, Collins DR. 2000. Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20:2701-2710.
76. Paré D, Collins DR, Pelletier JG. 2002. Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6:306-314.
77. Paré D, Royer S, Smith Y, Lang EJ. 2003. Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann N Y Acad Sci 985:78-91.
78. Paspalas CD, Papadopoulos GC. 2001. Serotoninergic afferents preferentially innervate distinct subclasses of peptidergic interneurons in the rat visual cortex. Brain Res 891:158-167.
79. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
80. Peters A, Harriman KM. 1988. Enigmatic bipolar cell of rat visual cortex. J. Comp Neurol 267:409-432.
81. Peters A, Harriman KM. 1992 Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. III. Origins and frequency of occurrence of the terminals. J Neurocytol 21:679-692.
82. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system. New York: Oxford University Press.
83. Pollandt S, Drephal C, Albrecht D. 2003. 8-OH-DPAT suppresses the induction of LTP in brain slices of the rat lateral amygdala. Neuroreport 14:895-897.
84. Rainnie DG. 1999. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69-85.
85. Rainnie DG. 2003. Inhibitory and excitatory circuitries in amygdala nuclei: a synopsis of session II. Ann N Y Acad Sci 985:59-66.
86. Rainnie DG, Asprodini EK, Shinnick-Gallagher P. 1993. Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69:1350-1361.
87. Rainnie DG, Mania I, Mascagni F, McDonald AJ. 2006. Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498:142-161.
88. Rauch SL, Shin LM, Wright CI. 2003. Neuroimaging studies of amygdala function in anxiety disorders. Ann N Y Acad Sci 985:389-410.
89. Rehfeld JF. 1978 Localisation of gastrins to neuro- and adenohypophysis. Nature 271:771-773.
90. Rehfeld JF, Lundberg JM. 1983. Cholecystokinin in feline vagal and sciatic nerves: concentration, molecular form and transport velocity. Brain Res 275:341-347.
91. 1A and preterminal axonal localization of 5-HT1B serotonin receptors in adult rat brain. J Comp Neurol 417:181-194.
92. 2A receptors in the human and nonhuman primate amygdala. Program No 203.17. Abstract viewer/Itinerary Planner. Washington DC: Society for Neuroscience.
93. Rueter LE, Jacobs BL. 1996. A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res 739:57-69.
94. Sadikot AF, Parent A. 1990. The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study. Neuroscience 36:431-447.
95. Seguela P, Watkins KC, Descarries L. 1989. Ultrastructural relationships of serotonin axon terminals in the cerebral cortex of the adult rat. J Comp Neurol 289:129-142.
96. Seidenbecher T, Laxmi TR, Stork O, Pape HC. 2003. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846-850.
97. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA. 2001. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 50:651-658.
98. Shinnick-Gallagher P, Pitkanen A, Shekhar, A, Cahill, L. 2003. The amygdala in brain function: basic and clinical approaches. Ann N Y Acad Sci. Vol. 985. New York: The New York Academy of Sciences.
99. Smiley JF, Goldman-Rakic PS. 1996. Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurons as demonstrated by serial section electron microscopy. J Comp Neurol 367: 431-443.
100. Smiley JF, Morrell F, Mesulam MM. 1997. Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp Neurol 144:361-368.
101. Smith Y, Paré D. 1994. Intra-amygdaloid projections of the lateral nucleus in the cat: PHA-L anterograde labeling combined with postembedding GABA and glutamate immunocytochemistry. J Comp Neurol 342:232-248.
102. Smith Y, Paré J-F, Paré, D. 2000. Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J Comp Neurol 416:496-508.
103. Sosulina L, Meis S, Seifert G, Steinhauser C, Pape HC. 2006. Classification of projection neurons and interneurons in the rat lateral amygdala based upon cluster analysis. Mol Cell Neurosci 33:57-67.
104. Stefanacci L, Farb CR, Pitkänen A, Go G, LeDoux JE, Amaral DG. 1992. Projections from the lateral nucleus to the basal nucleus of the amygdala: a light and electron microscopic PHA-L study in the rat. J Comp Neurol 323:586-601.
105. Stein C, Davidowa H, Albrecht D. 2000. 5-HT(1A) receptor-mediated inhibition and 5-HT(2) as well as 5-HT(3) receptor-mediated excitation in different subdivisions of the rat amygdala. Synapse 38:328-337.
106. Steinbusch HW. 1981. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618.
107. Stutzmann GE, LeDoux JE. 1999. GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 19:RC8.
108. Sur C, Betz H, Schloss P. 1996. Immunocytochemical detection of the serotonin transporter in rat brain. Neuroscience 73:217-231.
109. Tork I. 1990. Anatomy of the serotonergic system. Ann N Y Acad Sci 600:9-34.
110. Umbriaco D, Garcia S, Beaulieu C, Descarries L. 1995. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5:605-620.
111. Van Bockstaele EJ, Chan J, Pickel VM. 1996. Pre- and postsynaptic sites for serotonin modulation of GABA-containing neurons in the shell region of the rat nucleus accumbens. J Comp Neurol 371:116-128.
112. Van Haeften T, Wouterlood FG. 2000. Neuroanatomical tracing at high resolution. J Neurosci Methods 103:107-116.
113. Wang RY, Aghajanian GK. 1982. Correlative firing patterns of serotonergic neurons in rat dorsal raphe nucleus. J Neurosci 2:11-16.
114. Washburn MS, Moises HC. 1992. Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro. J Neurosci 12:4066-4079.
115. Woodruff AR, Sah P. 2007. Networks of parvalbumin-positive interneurons in the basolateral amygdala. J Neurosci 27:553-563.
116. Zald DH. 2003. The human amygdala and the emotional evaluation of sensory stimuli. Brain Res Rev 41:88-123.
117. Zangrossi H Jr, Graeff FG. 1994. Behavioral effects of intra-amygdala injections of GABA and 5-HT in the elevated plus-maze. Braz J Med Biol Res 27:2453-2456.