Differential postsynaptic compartments in the laterocapsular division of the central nucleus of amygdala for afferents from the parabrachial nucleus and the basolateral nucleus in the rat

Journal of Comparative Neurology

Volumn 518, Issue 23, 2010, Pages 4771-4791

  Dong, Yu Lin ^a,b   Fukazawa, Yugo ^a   Wang, Wen ^a,b   Kamasawa, Naomi ^a   Shigemoto, Ryuichi ^a,c  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

AMPA receptor; Dendritic shaft; Nociceptive amygdala; Postsynaptic density; SDS FRL; Spine

Indexed keywords

AMPA RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GOLD; LENTIVIRUS VECTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL NUCLEUS; BRAIN; CELL DENSITY; CONTROLLED STUDY; DENDRITE; EXCITATION; FREEZE FRACTURE; MALE; NERVE FIBER; NOCICEPTION; NONHUMAN; PARABRACHIAL NUCLEUS; POLYACRYLAMIDE GEL ELECTROPHORESIS; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPSE; ULTRASTRUCTURE;

AFFERENT PATHWAYS; AMYGDALA; ANIMALS; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS; RATS; RATS, WISTAR; SYNAPSES;

EID: 77958599508     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22487     Document Type: Article

References (127)

1. Antal M, Fukazawa Y, Eördögh M, Muszil D, Molnár E, Itakura M, Takahashi M, Shigemoto R. 2008. Numbers, densities, and colocalization of AMPA- and NMDA-type glutamate receptors at individual synapses in the superficial spinal dorsal horn of rats. J Neurosci 28: 9692-9701.
2. Asan E. 1995. The adrenergic innervation of the rat central amygdaloid nucleus: a light and electron microscopic immunocytochemical study using phenylethanolamine N-methyltransferase as a marker. Anat Embryol 192: 471-481.
3. Asan E. 1997. Ultrastructural features of tyrosine-hydroxylase-immunoreactive afferents and their targets in the rat amygdala. Cell Tissue Res 288: 449-469.
4. Augustine JR. 1996. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22: 229-244.
5. Bernard JF, Bandler R. 1998. Parallel circuits for emotional coping behaviour: new pieces in the puzzle. J Comp Neurol 401: 429-436.
6. Bernard JF, Besson JM. 1990. The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 63: 473-490.
7. Bernard JF, Huang GF, Besson JM. 1992. Nucleus centralis of the amygdala and the globus pallidus ventralis: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 68: 551-569.
8. Bernard JF, Alden M, Besson JM. 1993. The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329: 201-229.
9. Bird GC, Lash LL, Han JS, Zou X, Willis WD, Neugebauer V. 2005. Protein kinase A-dependent enhanced NMDA receptor function in pain-related synaptic plasticity in rat amygdala neurones. J Physiol 564: 907-921.
10. Bishop GA, Chang HT, Kitai ST. 1982. Morphological and physiological properties of neostriatal neurons: an intracellular horseradish peroxidase study in the rat. Neuroscience 7: 179-191.
11. Block CH, Hoffman G, Kapp BS. 1989. Peptide-containing pathways from the parabrachial complex to the central nucleus of the amygdala. Peptides 10: 465-471.
12. Boon JA, Milsom WK. 2008. NMDA receptor-mediated processes in the parabrachial/Kölliker fuse complex influence respiratory responses directly and indirectly via changes in cortical activation state. Respir Physiol Neurobiol 162: 63-72.
13. Bourgeais L, Gauriau C, Monconduit L, Villanueva L, Bernard JF. 2003. Dendritic domains of nociceptive-responsive parabrachial neurons match terminal fields of lamina I neurons in the rat. J Comp Neurol 464: 238-256.
14. Bredt DS, Nicoll RA. 2003. AMPA receptor trafficking at excitatory synapses. Neuron 40: 361-379.
15. Carlsen J, Heimer L. 1988. The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441: 377-380.
16. Chao T, Pham K, Steward O, Gupta R. 2008. Chronic nerve compression injury induces a phenotypic switch of neurons within the dorsal root ganglia. J Comp Neurol 506: 180-193.
17. Chieng BC, Christie MJ, Osborne PB. 2006. Characterization of neurons in the rat central nucleus of the amygdala: cellular physiology, morphology, and opioid sensitivity. J Comp Neurol 497: 910-927.
18. de Lacalle S, Saper CB. 2000. Calcitonin gene-related peptide-like immunoreactivity marks putative visceral sensory pathways in human brain. Neuroscience 100: 115-130.
19. Delaney AJ, Crane JW, Sah P. 2007. Noradrenaline modulates transmission at a central synapse by a presynaptic mechanism. Neuron 56: 880-892.
20. D'Hanis W, Linke R, Yilmazer-Hanke DM. 2007. Topography of thalamic and parabrachial calcitonin gene-related peptide (CGRP) immunoreactive neurons projecting to subnuclei of the amygdala and extended amygdala. J Comp Neurol 505: 268-291.
21. Dubé L, Smith AD, Bolam JP. 1988. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267: 455-471.
22. Fujimoto K. 1995. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci 108: 3443-3449.
23. Fukata M, Nakagawa M, Itoh N, Kawajiri A, Yamaga M, Kuroda S, Kaibuchi K. 2001. Involvement of IQGAP1, an effector of Rac1 and Cdc42 GTPases, in cell-cell dissociation during cell scattering. Mol Cell Biol 21: 2165-2183.
24. Fundytus ME. 2001. Glutamate receptors and nociception: implications for the drug treatment of pain. CNS Drugs 15: 29-58.
25. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. 2004. Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience 125: 615-623.
26. Gray TS, Cassell MD, Williams TH. 1982. Synaptology of three peptidergic neuron types in the central nucleus of the rat amygdala. Peptides 3: 273-281.
27. Han JS, Li W, Neugebauer V. 2005. Critical role of calcitonin gene-related peptide 1 receptors in the amygdala in synaptic plasticity and pain behavior. J Neurosci 25: 10717-10728.
28. Han JS, Adwanikar H, Li Z, Ji G, Neugebauer V. 2010. Facilitation of synaptic transmission and pain responses by CGRP in the amygdala of normal rats. Mol Pain 6: 10.
29. Harrigan EA, Magnuson DJ, Thunstedt GM, Gray TS. 1994. Corticotropin releasing factor neurons are innervated by calcitonin gene-related peptide terminals in the rat central amygdaloid nucleus. Brain Res Bull 33: 529-534.
30. Harris KM, Landis DM. 1986. Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 19: 857-872.
31. Helmeke C, Ovtscharoff W Jr, Poeggel G, Braun K. 2001. Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb Cortex 11: 717-727.
32. Herbert H, Moga MM, Saper CB. 1990. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 293: 540-580.
33. Honkaniemi J. 1992. Colocalization of peptide- and tyrosine hydroxylase-like immunoreactivities with Fos-immunoreactive neurons in rat central amygdaloid nucleus after immobilization stress. Brain Res 598: 107-113.
34. Honkaniemi J, Pelto-Huikko M, Isola J, Rechardt L. 1990. Simultaneous localization of calcitonin gene-related peptide and neurotensin in rat central amygdaloid nucleus. Neurosci Lett 113: 1-6.
35. Ikeda R, Takahashi Y, Inoue K, Kato F. 2007. NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain 127: 161-172.
36. Jasmin L, Burkey AR, Card JP, Basbaum AI. 1997. Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-) parabrachio-amygdaloid, in the rat. J Neurosci 17: 3751-3765.
37. Ji G, Horváth C, Neugebauer V. 2009. NR2B receptor blockade inhibits pain-related sensitization of amygdala neurons. Mol Pain 5: 21.
38. Jolkkonen E, Miettinen R, Pitkänen A. 2001. Projections from the amygdalo-piriform transition area to the amygdaloid complex: a PHA-l study in rat. J Comp Neurol 432: 440-465.
39. Kits KS, Dreijer AM, Lodder JC, Borgdorff A, Wadman WJ. 1997. High intracellular calcium levels during and after electrical discharges in molluscan peptidergic neurons. Neuroscience 79: 275-284.
40. Kresse A, Jacobowitz DM, Skofitsch G. 1995. Detailed mapping of CGRP mRNA expression in the rat central nervous system: comparison with previous immunocytochemical findings. Brain Res Bull 36: 261-274.
41. Kruger L, Sternini C, Brecha NC, Mantyh PW. 1988. Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection. J Comp Neurol 273: 149-162.
42. Kulik A, Nakadate K, Nyíri G, Notomi T, Malitschek B, Bettler B, Shigemoto R. 2002. Distinct localization of GABAB receptors relative to synaptic sites in the rat cerebellum and ventrobasal thalamus. Eur J Neurosci 15: 291-307.
43. Lacey CJ, Bolam JP, Magill PJ. 2007. Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27: 4374-4384.
44. LeDoux JE. 1995. Emotion: clues from the brain. Annu Rev Psychol 46: 209-235.
45. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
46. Li W, Neugebauer V. 2004. Block of NMDA and non-NMDA receptor activation results in reduced background and evoked activity of central amygdala neurons in a model of arthritic pain. Pain 110: 112-122.
47. Lopez de Armentia M, Sah P. 2004. Firing properties and connectivity of neurons in the rat lateral central nucleus of the amygdala. J Neurophysiol 92: 1285-1294.
48. Malenka RC. 2003. Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci 1003: 1-11.
49. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126.
50. Maren S. 2005. Synaptic mechanisms of associative memory in the amygdala. Neuron 47: 783-786.
51. Martin TF. 1994. The molecular machinery for fast and slow neurosecretion. Curr Opin Neurobiol 4: 626-632.
52. Masugi-Tokita M, Shigemoto R. 2007. High-resolution quantitative visualization of receptors at central synapses. Curr Opin Neurobiol 17: 387-393.
53. Masugi-Tokita M, Tarusawa E, Watanabe M, Molnár E, Fujimoto K, Shigemoto R. 2007. Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci 27: 2135-2144.
54. Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP. 1996. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of corti. J Neurosci 16: 4457-4467.
55. Mattes H, Lingenhoehl K, Kalkman H, Auberson Y, Renaud J, Schmutz M, Orain D. 2006. AMPA receptor antagonists: potential therapeutic applications. Recent Patt CNS Drug Discov 1: 247-259.
56. McDonald AJ. 1982. Cytoarchitecture of the central amygdaloid nucleus of the rat. J Comp Neurol 208: 401-418.
57. McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog Neurobiol 55: 257-332.
58. McWilliams LA, Cox BJ, Enns MW. 2003. Mood and anxiety disorders associated with chronic pain: an examination in a nationally representative sample. Pain 106: 127-133.
59. McWilliams LA, Goodwin RD, Cox BJ. 2004. Depression and anxiety associated with three pain conditions: results from a nationally representative sample. Pain 111: 77-83.
60. Millan MJ. 1999. The induction of pain: an integrative review. Prog Neurobiol 57: 1-164.
61. Miyamoto E. 2006. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100: 433-442.
62. Neugebauer V. 2006. Chapter 11 Subcortical processing of nociceptive information: basal ganglia and amygdala. Hdbk Clin Neurol 81: 141-158.
63. Neugebauer V, Li W. 2002. Processing of nociceptive mechanical and thermal information in central amygdala neurons with knee-joint input. J Neurophysiol 87: 103-112.
64. Neugebauer V, Li W. 2003. Differential sensitization of amygdala neurons to afferent inputs in a model of arthritic pain. J Neurophysiol 89: 716-727.
65. Neugebauer V, Li W, Bird GC, Bhave G, Gereau RW4th. 2003. Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J Neurosci 23: 52-63.
66. Neugebauer V, Li W, Bird GC, Han JS. 2004. The amygdala and persistent pain. Neuroscientist 10: 221-234.
67. Nikolakopoulou AM, Davies HA, Stewart MG. 2006. Passive avoidance training decreases synapse density in the hippocampus of the domestic chick. Eur J Neurosci 23: 1054-1062.
68. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somomgyi P. 1998. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21: 545-559.
69. Oliver KR, Wainwright A, Heavens RP, Hill RG, Sirinathsinghji DJ. 1998. Distribution of novel CGRP1 receptor and adrenomedullin receptor mRNAs in the rat central nervous system. Brain Res Mol Brain Res 57: 149-154.
70. Ottersen OP. 1980. Afferent connections to the amygdaloid complex of the rat and cat: I. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194: 267-289.
71. Ottersen OP. 1981. Afferent connections to the amygdaloid complex of the rat with some observations in the cat. II. Afferents from the lower brain stem. J Comp Neurol 202: 335-356.
72. Ottersen OP, Ben-Ari Y. 1979. Afferent connections to the amygdaloid complex of the rat and cat. III. Projection from the thalamus. J Comp Neurol 187: 401-424.
73. 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.
74. Park Y, Kim KT. 2009. Short-term plasticity of small synaptic vesicle (SSV) and large dense-core vesicle (LDCV) exocytosis. Cell Signal 21: 1465-1470.
75. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KG, Kamasawa N, Yasumura T, Rash JE. 2003. Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23: 7489-7503.
76. Phelps EA, LeDoux JE. 2005. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48: 175-187.
77. Pitkänen A. 2000. Connectivity of the rat amygdaloid complex. In: Aggleton JP, editor. The amygdala: a functional analysis. Oxford, United Kingdom: Oxford Univerwsity Press. p 31-115.
78. Pitkänen A, Amaral DG. 1998. Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398: 431-458.
79. Pitkänen A, Stefanacci L, Farb CR, Go GG, LeDoux JE, Amaral DG. 1995. Intrinsic connections of the rat amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 356: 288-310.
80. Pitkänen A, Savander V, LeDoux JE. 1997. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20: 517-523.
81. Planells-Cases R, Lerma J, Ferrer-Montiel A. 2006. Pharmacological intervention at ionotropic glutamate receptor complexes. Curr Pharm Des 12: 3583-3596.
82. Poliacek I, Halasova E, Jakus J, Murin P, Barani H, Stransky A, Bolser DC. 2007. Brainstem regions involved in the expiration reflex. A c-fos study in anesthetized cats. Brain Res 1184: 168-177.
83. Price DD. 2000. Psychological and neural mechanisms of the affective dimension of pain. Science 288: 1769-1772.
84. Price DD. 2002. Central neural mechanisms that interrelate sensory and affective dimensions of pain. Mol Intervent 2: 339, 392-403.
85. Puelles L. 2001. Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium. Philos Trans R Soc Lond B Biol Sci 356: 1583-1598.
86. Rhudy JL, Meagher MW. 2003. Negative affect: effects on an evaluative measure of human pain. Pain 104: 617-626.
87. Rizvi TA, Ennis M, Behbehani MM, Shipley MT. 1991. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303: 121-131.
88. Royet JP. 1991. Stereology: a method for analyzing images. Prog Neurobiol 37: 433-474.
89. Rusakov DA, Harrison E, Stewart MG. 1998. Synapses in hippocampus occupy only 1-2% of cell membranes and are spaced less than half-micron apart: a quantitative ultrastructural analysis with discussion of physiological implications. Neuropharmacology 37: 513-521.
90. Russchen FT. 1982. Amygdalopetal projections in the cat. I. Subcortical afferent connections. A study with retrograde tracing techniques. J Comp Neurol 207: 157-176.
91. Sah P, Lopez de Armentia M. 2003. Excitatory synaptic transmission in the lateral and central amygdala. Ann N Y Acad Sci 985: 67-77.
92. Sah P, Faber ES, Lopez de Armentia M, Power J. 2003. The amygdaloid complex: anatomy and physiology. Physiol Rev 83: 803-834.
93. Salio C, Lossi L, Ferrini F, Merighi A. 2006. Neuropeptides as synaptic transmitters. Cell Tissue Res 326: 583-598.
94. Sandri C, Akert K, Livingston RB, Moor H. 1972. Particle aggregations at specialized sites in freeze-etched postsynaptic membranes. Brain Res 41: 1-16.
95. Sarhan M, Freund-Mercier MJ, Veinante P. 2005. Branching patterns of parabrachial neurons projecting to the central extend amygdala: single axonal reconstructions. J Comp Neurol 491: 418-442.
96. Savander V, Go CG, LeDoux JE, Pitkänen A. 1995. Intrinsic connections of the rat amygdaloid complex: projections originating in the basal nucleus. J Comp Neurol 361: 345-368.
97. Savander V, Go CG, Ledoux JE, Pitkänen A. 1996. Intrinsic connections of the rat amygdaloid complex: projections originating in the accessory basal nucleus. J Comp Neurol 374: 291-313.
98. Schiess MC, Callahan PM, Zheng H. 1999. Characterization of the electrophysiological and morphological properties of rat central amygdala neurons in vitro. J Neurosci Res 58: 663-673.
99. Schwaber JS, Sternini C, Brecha NC, Rogers WT, Card JP. 1988. Neurons containing calcitonin gene-related peptide in the parabrachial nucleus project to the central nucleus of the amygdala. J Comp Neurol 270: 416-426.
100. Scott TR, Small DM. 2009. The role of the parabrachial nucleus in taste processing and feeding. Ann N Y Acad Sci 1170: 372-377.
101. Shi C, Davis M. 1999. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci 19: 420-430.
102. Shimada S, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, Maclntyre I, Tohyama M. 1985. Calcitonin gene-related peptidergic projection from the parabrachial area to the forebrain and diencephalon in the rat: an immunohistochemical analysis. Neuroscience 16: 607-616.
103. Shimada S, Inagaki S, Narita N, Takagi H. 1992. Synaptic contacts between CGRP-immunoreactive terminals and enkephalin-immunoreactive neurons in the central amygdaloid nucleus of the rat. Neurosci Lett 134: 243-246.
104. Shinohara Y, Hirase H, Watanabe M, Itakura M, Takahashi M, Shigemoto R. 2008. Left-right asymmetry of the hippocampus synapses with differential subunit allocation of glutamate receptors. Proc Natl Acad Sci U S A 105: 19498-19503.
105. Sliwinska-Kowalska M, Parakkal M, Schneider ME, Fex J. 1989. CGRP-like immunoreactivity in the guinea pig organ of corti: a light and electron microscopy study. Hear Res 42: 83-95.
106. Smith Y, Raju D, Nanda B, Pare JF, Galvan A, Wichmann T. 2009. The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states. Brain Res Bull 78: 60-68.
107. Stalnaker TA, Berridge CW. 2003. AMPA receptor stimulation within the central nucleus of the amygdala elicits a differential activation of central dopaminergic systems. Neuropsychopharmacology 28: 1923-1934.
108. Swanson LW, Petrovich GD. 1998. What is the amygdala? Trends Neurosci 21: 323-331.
109. Takano K, Kato F. 2003. Inspiration-promoting vagal reflex in anaesthetized rabbits after rostral dorsolateral pons lesion. J Physiol 550: 973-983.
110. Takeuchi Y, Xie Q, Miki T, Matsumoto Y, Satriotomo I, Li HP, Gu H. 2004. Parabrachial inputs to Fos-immunoreactive neurons in the lateral central nucleus of amygdala activated by hypotension: a light and electron microscopic study in the rat. Brain Res Bull 64: 171-180.
111. Tallent MK. 2008. Presynaptic inhibition of glutamate release by neuropeptides: use-dependent synaptic modification. Results Probl Cell Differ 44: 177-200.
112. Tanaka J, Matsuzaki M, Tarusawa E, Momiyama A, Molnar E, Kasai H, Shigemoto R. 2005. Number and density of AMPA receptors in single synapses in immature cerebellum. J Neurosci 25: 799-807.
113. Tarusawa E, Matsui K, Budisantoso T, Molnár E, Watanabe M, Matsui M, Fukazawa Y, Shigemoto R. 2009. Input-specific intrasynaptic arrangements of ionotropic glutamate receptors and their impact on postsynaptic responses. J Neurosci 29: 12896-12908.
114. Torashima T, Okoyama S, Nishizaki T, Hirai H. 2006. In vivo transduction of murine cerebellar Purkinje cells by HIV-derived lentiviral vectors. Brain Res 1082: 11-22.
115. Triller A, Choquet D. 2005. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28: 133-139.
116. van Rossum D, Hanisch UK, Quirion R. 1997. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides and their receptors. Neurosci Biobehav Rev 21: 649-678.
117. Verhage M, McMahon HT, Ghijsen WE, Boomsma F, Scholten G, Wiegant VM, Nicholls DG. 1991. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6: 517-524.
118. Watanabe H, Yamamoto TY. 1981. Freeze fracture study on three types of synapses in the Xenopus spinal cord. J Comp Neurol 198: 249-263.
119. Watanabe T, Nakagawa T, Yamamoto R, Maeda A, Minami M, Satoh M. 2002. Involvement of glutamate receptors within the central nucleus of the amygdala in naloxone-precipitated morphine withdrawal-induced conditioned place aversion in rats. Jpn J Pharmacol 88: 399-406.
120. Willis WD. 2001. Role of neurotransmitters in sensitization of pain responses. Ann N Y Acad Sci 933: 142-156.
121. Xia J, Chung HJ, Wihler C, Huganir RL, Linder DJ. 2000. Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 28: 499-510.
122. Yamamoto T, Takemura M, Inui T, Torii K, Maeda N, Ohmoto M, Matsumoto I, Abe K. 2009. Functional organization of the rodent parabrachial nucleus. Ann N Y Acad Sci 1170: 378-382.
123. Yamano M, Hillyard CJ, Girgis S, Emson PC, MacIntyre I, Tohyama M. 1988. Projection of neurotensin-like immunoreactive neurons from the lateral parabrachial area to the central amygdaloid nucleus of the rat with reference to the coexistence with calcitonin gene-related peptide. Exp Brain Res 71: 603-610.
124. Yashiro K, Philpot BD. 2008. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55: 1081-1094.
125. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhao M. 2005. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47: 859-872.
126. Zhuo M. 2009. Plasticity of NMDA receptor NR2B subunit in memory and chronic pain. Mol Brain 2: 4.
127. Zinebi F, McKernan M, Shinnick-Gallagher P. 2002. Expression of fear-conditioning is accompanied by increased paired-pulse depression within the amygdala. Pharmacol Biochem Behav 71: 393-400.