Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: A critical involvement of the amygdala

Biological Psychiatry

Volumn 46, Issue 9, 1999, Pages 1140-1152

  Ferry, Barbara ^a   Roozendaal, Benno ^a   McGaugh, James L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

adrenoceptor; adrenoceptor; Basolateral amygdala; Memory storage; Norepinephrine; Stress hormones

Indexed keywords

8 BROMO CYCLIC AMP; ADRENALIN; ALPHA 1 ADRENERGIC RECEPTOR; AMPHETAMINE; ATENOLOL; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CLENBUTEROL; CORTICOSTEROID; DEXAMETHASONE; HYDROXYAMPHETAMINE; NORADRENALIN; PHENYLEPHRINE; PROPRANOLOL; YOHIMBINE;

AMYGDALOID NUCLEUS; AVOIDANCE BEHAVIOR; BASOLATERAL MEMBRANE; BEHAVIOR; LONG TERM MEMORY; MAZE TEST; MEMORY CONSOLIDATION; MICRODIALYSIS; NEUROPHYSIOLOGY; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; REVIEW;

ADRENAL CORTEX HORMONES; AMYGDALA; ANIMALS; HUMANS; MEMORY; NOREPINEPHRINE; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, ADRENERGIC, BETA;

EID: 0033232494     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3223(99)00157-2     Document Type: Review

References (123)

1. Arbilla S., Langer S.Z. Morphine and beta-endorphin inhibit the release of noradrenaline from cerebral cortex but not of dopamine from rat striatum. Nature. 271:1978;559-561.
2. Brioni J.D., McGaugh J.L. Posttraining administration of GABAergic antagonists enhance retention of aversively motivated tasks. Psychopharmacology. 96:1988;505-510.
3. Brioni J.D., Nagahara A.H., McGaugh J.L. Involvement of the amygdala GABAergic system in the modulation of memory storage. Brain Res. 487:1989;105-112.
4. Cahill L., McGaugh J.L. Amygdaloid complex lesions differentially affect retention of tasks using apetitive and aversive reinforcement. Behav Neurosci. 104:1990;532-543.
5. Castellano C. Effects of morphine and heroin on discrimination learning and consolidation in mice. Psychopharmacology. 73:1975;291-295.
6. Christianson S.V. Remembering emotional events Potential mechanisms . Christianson S.V. The Handbook of Emotion and Memory Research and Theory . 1992;307-340 Lawrence Erlbaum Associates Inc, Hillsdale.
7. Da Cunha C, Roozendaal B, Vazdarjanova A, McGaugh JL (1999): Microinfusions of flumazenil into the basolateral but not the central nucleus of the amygdala enhance memory consolidation in rats. Neurobiol Learn Mem 72:1-7.
8. Davis M. The role of the amygdala in conditioned fear. Aggleton J. The Amygdala. 1992;255-306 Wiley-Liss, Inc, New York.
9. Decker M.W., Introini-Collison I.B., McGaugh J.L. Effects of naloxone on Morris water maze learning in the rat Enhanced acquisition with pretraining but not posttraining administration . Psychobiology. 17:1981;270-275.
10. De Quervain D.J.F., Roozendaal B., McGaugh. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature. 394:1998;787-790.
11. de Souza-Silva M.A., Tomaz C. Amnesia after diazepam infusion into the basolateral but not central amygdala of Rattus norveticus. Neuropsychobiology. 32:1995;31-36.
12. Dews P.B., Morse W.H. Behavioral pharmacology. Ann Rev Pharmacol. 1:1961;145-174.
13. Doty B.A., Doty L.A. Facilitative effects of amphetamine on avoidance conditioning in relation to age and problem difficulty. Psychopharmacologia. 9:1966;234-241.
14. Evangelista A.M., Gattoni R.C., Izquierdo I. Effect of amphetamine, nicotine and hexamethonium on performance of a conditioned response during acquisition and retention trials. Pharmacology. 3:1970;91-96.
15. Ferry B, McGaugh JL (1999): Clenbuterol administration into the basolateral amygdala posttraining enhances retention in an inhibitory avoidance task. Neurobiol Learn Mem 72:8-12.
16. 1-adrenergic receptors in the basolateral amygdala in modulation of memory storage. Eur J Pharmacol 372:9-16.
17. 1-adrenoceptors. J Neurosci 19:5119-5123.
18. Ferry B., Sandner G., Di Scala G. Neuroanatomical and functional specificity of basolateral amygdaloid nucleus in taste potentiated odor aversion. Neurobiol Learn Mem. 64:1995;169-180.
19. Ferry B, Wirth S, Di Scala G (1999): Functional interaction between entorhinal cortex and basolateral amygdala during trace conditioning of odor aversion in the rat. Behav Neurosci 113:118-125.
20. Flood J.F., Vidal D., Bennett E.L., Orme A.E., Vasquez S., Jarvik M.E. Memory facilitating and anti-amnestic effects of glucocorticoids. Pharmacol Biochem Behav. 8:1978;81-87.
21. Gallagher M., Kapp B.S. Manipulation of opiate activity in the amygdala alters memory processes. Life Sci. 23:1978;1973-1978.
22. Gallagher M., Kapp B.S., Musty R.E., Driscoll P.A. Memory formation Evidence for a specific neurochemical system in the amygdala . Science. 198:1977;423-425.
23. Gallagher M., Rapp P.S., Fanelli R.J. Opiate antagonist facilitation of time-dependent memory processes Dependence upon intact norepinephrine function . Brain Res. 347:1985;284-290.
24. Galvez R., Mesches M., McGaugh J.L. Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiol Learn Mem. 66:1996;253-257.
25. Gold P.E., van Buskirk R.B. Facilitation of time-dependent memory processes with posttrial amygdala stimulation effect on memory varies with footshock level . Brain Res. 86:1975;509-513.
26. Gold P.E., van Burskirk R.B. Posttraining brain norepinephrine concentrations Correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing . Behav Biol. 25:1978;509-520.
27. Gold P.E., van Buskirk R.B., McGaugh J.L. Effects of hormones on time-dependent memory storage processes. Prog Brain Res. 42:1975;210-211.
28. Härfstrand A., Fuxe K., Cintra A., Agnati L., Mzini L., Wikstrom A.C., et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc Natl Acad Sci. 83:1986;9779-9783.
29. Hatfield T., Graham P.W., Gallagher M. Taste-potentiated odor aversion learning Role of the amygdaloid basolateral complex and central nucleus . Behav Neurosci. 106:1992;286-293.
30. Hatfield T., McGaugh J.L. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol Learn Mem. 71:1999;232-239.
31. Hatfield T, Spanis C, McGaugh JL (in press): Response of amygdala norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC. Brain Res.
32. Haycock J.W., van Burskirk R., McGaugh J.L. Effects of diethyldithiocarbamate on memory processes in mice A neurobiological analysis . Behav Biol. 20:1977;281-310.
33. Herz A. Drugs and the conditioned avoidance response. Intl Rev Neurobiol. 2:1960;229-277.
34. Huang C.C., Tsai J.J., Gean P.W. Actions of isoproterenol on amygdala neurons in vitro. Chin J Physiol. 37:1994;73-78.
35. Ikegaya Y., Saito H., Abe K. Attenuated hippocampal long-term potentiation in basolateral amygdala lesioned rats. Brain Res. 656:1994;157-164.
36. Ikegaya Y., Saito H., Abe K. Requirement of basolateral amygdala neuron activity for the induction of long-term potentiation in the dentate gyrus in vivo. Brain Res. 671:1995;351-354.
37. Ikegaya Y., Saito H., Abe K. High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo. Neurosci Res. 22:1995;203-207.
38. Ikegaya Y., Saito H., Abe K., Nakanishi K. Amygdala β-noradrenergic influence on hippocampal long-term potentiation in vivo. NeuroReport. 8:1997;3143-3146.
39. Introini I.B., Baratti C.M. The impairment of retention induced by β-endorphin in mice may be mediated by a reduction of central cholinergic activity. Behav Neural Biol. 41:1984;152-163.
40. Introini-Collison I.B., Arai Y., McGaugh J.L. Stria terminalis lesions attenuate the effects of posttraining oxotremorine and atropine on retention. Psychobiology. 17:1989;397-401.
41. Introini-Collison I.B., Baratti C.M. Opioid peptidergic systems modulate the activity of β-adrenergic mechanisms during memory consolidation processes. Behav Neural Biol. 46:1986;227-241.
42. Introini-Collison I.B., Ford L., McGaugh J.L. Memory impairment induced by intra-amygdala β-endorphin is mediated by noradrenergic influences. Neurobiol Learn Mem. 63:1995;200-205.
43. Introini-Collison I.B., McGaugh J.L. Epinephrine modulates long-term retention of an aversively-motivated discrimination task. Behav Neural Biol. 45:1986;358-365.
44. Introini-Collison I.B., McGaugh J.L. Naloxone and beta-endorphin alter the effects of post-training epinephrine on retention of an inhibitory avoidance response. Psychopharmacology. 92:1987;229-235.
45. Introini-Collison I.B., Miyazaki B., McGaugh J.L. Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology. 104:1991;541-544.
46. Introini-Collison I.B., Nagahara A.H., McGaugh J.L. Memory-enhancement with intra-amygdala posttraining naloxone is blocked by concurrent administration of propranolol. Brain Res. 476:1989;94-101.
47. Introini-Collison I.B., Saghafi D., Novack G., McGaugh J.L. Memory enhancing effects of posttraining dipivefrin and epinephrine Involvement of peripheral and central adrenergic receptors . Brain Res. 572:1992;81-86.
48. Izquierdo I. Effect of naloxone and morphine on various forms of memory in the rat Possible role endogenous opiate mechanisms in memory consolidation . Psychopharmacology. 66:1979;199-203.
49. Jensen R.A., Martinez J.L., Vasquez B.J., McGaugh J.L., McGuinness T. Amnesia produced by intraventricular administration of diethyldithiocarbamate. Neurosci Abst. 3:1977;235.
50. Kalia M., Sullivan J.M. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol. 211:1982;248-264.
51. Kety S. Brain catecholamines, affective states and memory. McGaugh J.L. The Chemistry of Mood, Motivation and Memory. 1972;65-80 Plenum Press, New York.
52. Kim M., Davis M. Electrolytic lesions of the amygdala block acquisition and expression of fear-potentiated startle even with extensive training but does not prevent reacquisition. Behav Neurosci. 7:1993;580-595.
53. Krivaneck J.A., McGaugh J.L. Facilitating effects of pre- and post-trial amphetamine administration on discriminating learning in mice. Agents Actions. 1:1969;36-42.
54. Langer S.Z. Presynaptic regulation of catecholamine release. Biochem Pharmacol. 23:1974;1793-1800.
55. Leblanc G.G., Ciaranello R.D. α-Noradrenergic potentiation of neurotransmitter-stimulated cAMP production in rat striatal slices. Brain Res. 293:1984;57-65.
56. LeDoux J.E. Emotion Clues from the brain . Ann Rev Psychol. 46:1995;209-235.
57. Liang K.C., Bennett C., McGaugh J.L. Peripheral epinephrine modulates the effects of posttraining amygdala stimulation on memory. Behav Brain Res. 15:1985;93-100.
58. Liang K., Chen L., Huang T.E. The role of amygdala norepinephrine in memory formation Involvement in the memory-enhancing effect of peripheral epinephrine . Chin J Physiol. 38:1995;81-91.
59. Liang K.C., Juler R., McGaugh J.L. Modulating effects of posttraining epinephrine on memory Involvement of the amygdala noradrenergic system . Brain Res. 368:1986;125-133.
60. Liang K.C., McGaugh J.L. Lesions of the stria terminalis attenuate the enhancing effect of posttraining epinephrine on retention of an inhibitory avoidance response. Behav Brain Res. 9:1983;49-58.
61. Liang K., McGaugh J.L., Yao H. Involvement of amygdala pathways in the influence of posttraining amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 508:1990;225-233.
62. Lupien S.J., McEwen B.S. The caute effects of corticosteroids on cognition Integration of animal and human model studies . Brain Res Rev. 24:1997;1-27.
63. Maren S. Overtraining does not mitigate contextual fear conditioning deficits produced by neurotoxic lesions of the basolateral amygdala. J Neurosci. 18:1998;3088-3097.
64. Martinez J.L. Jr, Jensen R.A., Messing R.B., Vasquez B.J., Soumireu-Mourat B., Geddes D., et al. Central and peripheral actions of amphetamine on memory storage. Brain Res. 182:1980;157-166.
65. Martinez J.L. Jr, Vasquez B.J., Rigter H., Messing R.B., Jensen R.A., Liang K.C., et al. Attenuation of amphetamine-induced enhancement of learning by adrenal demedullation. Brain Res. 195:1980;433-443.
66. Martinez J.L. Jr, Weinberger S.B., Schulteis G. Enkephalins and learning and memory A review of evidence for a site of action outside the blood brain barrier . Behav Neural Biol. 49:1988;192-221.
67. Mauk M.D., Madden J., Barchas J.D., Thompson R.F. Opiates and classical conditioning Selective abolition of conditioned responses by activation of opiate receptors within the central nervous system . Proc Natl Acad Sci. 79:1982;7598-7602.
68. McCarty R., Gold P.E. Plasma catecholamines effects of footshock level and hormonal modulators of memory storage . Horm Behav. 15:1981;168-182.
69. McEwen B.S., Sapolsky R.M. Stress and cognitive function. Curr Opin Neurobiol. 5:1995;205-216.
70. McGaugh J.L. Time dependent processes in memory storage. Science. 153:1966;1351-1358.
71. McGaugh J.L. Drug facilitation of learning and memory. Ann Rev Pharmacol. 13:1973;229-241.
72. McGaugh J.L. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage. Ann Rev Neurosci. 12:1989;255-287.
73. McGaugh J.L. Dissociating learning and performance Drug and hormone enhancement of memory storage . Brain Res Bull. 23:1989;339-345.
74. McGaugh J.L., Gold P.E. The effects of drugs and electrical stimulation of the brain on memory storage processes. Myers R.D., Drucker-Colin R.R. Neurohumoral Coding of Brain Function. 1974;189-206 Plenum Press, New York.
75. McGaugh J.L., Gold P.E., Handwerker M.J., Jensen R.A., Martinez J.L. Jr. Altering memory by electrical and chemical stimulation of the brain. Brazier M.A.B. Brain Mechanisms in Memory and Learning From the Single Neuron to Man . 1979;151-164 Raven, New York.
76. McGaugh JL, Herz MJ (1972): Memory Consolidation. San Francisco: Albion Publishing Company.
77. McGaugh J.L., Introini-Collison I.B., Nagahara A.H. Memory-enhancing effects of posttraining naloxone Involvement of β-adrenergic influences in the amygdaloid complex . Brain Res. 446:1988;37-49.
78. Meligeni J.A., Ledergerber S.A., McGaugh J.L. Norepinephrine attenuation of amnesia produced by diethyldithiocarbamate. Brain Res. 149:1978;155-164.
79. Mesches M., McGaugh J.L. Effects of D-amphetamine on extracellular norepinephrine levels in the amygdala of freely moving rats as measured by in vivo microdialysis. Soc Neurosci Abst. 17:1991;1398.
80. Morris R.G., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 297:1982;681-683.
81. Moser E., Moser M.B., Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci. 13:1993;3916-3925.
82. Mueller G.E., Pilzecker A. Experimentelle Beitrage zur lehre vom Gedachtniss. Zeitshrift fir Psychologie. 1:1900;1-288.
83. O'Donnell P., Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons Hippocampal gating of prefrontal cortical input . Behav Neural Biol. 62:1995;190-200.
84. Olton D.S., Becker J.T., Handelman G.E. Hippocampus, space, and memory. Behav Brain Sci. 2:1979;313-365.
85. Packard M.G., Cahill L., McGaugh J.L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci. 91:1994;8477-8481.
86. Packard M.G., McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks Further evidence for multiple memory systems . Behav Neurosci. 106:1992;439-446.
87. Packard M.G., McGaugh J.L. Inactivation of the hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem. 65:1996;65-72.
88. Packard M.G., Teather L. Amygdala modulation of multiple memory systems Hippocampus and caudate putamen . Neurobiol Learn Mem. 69:1998;163-203.
89. Packard M.G., Williams C., Cahill L., McGaugh J.L. The anatomy of memory modulatory system From periphery to brain . Spear N., Spear L., Woodruff M. Neurobehavioral Plasticity Leaning, Development and Response to Brain Insults . 1995;149-184 Lawrence Erlbaum Associates, Mahwah, NJ.
90. Parent M.B., Avila E., McGaugh J.L. Footshock facilitates the expression of aversively motivated memory in rats given post-training amygdala basolateral complex lesions. Brain Res. 676:1995;235-244.
91. Parent M.B., McGaugh J.L. Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance. Brain Res. 661:1994;97-103.
92. Parent M.B., Tomaz C., McGaugh J.L. Increased training in an aversively motivated task attenuate the memory impairing effects of posttraining N-methyl-D-aspartic acid-induced amygdala lesions. Behav Neurosci. 106:1992;791-799.
93. Parent M.B., West M., McGaugh J.L. Memory of rats with amygdala lesions induced 30 days after footshock-motivated escape training reflects degree of original training. Behav Neurosci. 6:1994;1080-1087.
94. Perkins J.P., Moore M.M. Characterization of the adrenergic receptors mediating a rise in cyclic 3′,5′-adenosine monophosphate in rat cerebral cortex. J Pharmacol Exp Ther. 185:1973;371-378.
95. Quirarte G.L., Galvez R., Roozendaal B., McGaugh J.L. Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs. Brain Res. 808:1998;134-140.
96. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci. 94:1997;14048-14053.
97. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid receptor antagonist infused into the basolateral amygdala inhibits the memory enhancing effects of the noradrenergic agonist infused clenbuterol. Soc Neurosci Abst. 23:1997;1314.
98. Roozendaal B., McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem. 65:1996;1-8.
99. Roozendaal B., McGaugh J.L. The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis. Brain Res. 709:1996;243-250.
100. Roozendaal B., McGaugh J.L. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci. 9:1997;76-83.
101. Roozendaal B, Nguyen BT, Power AE, McGaugh JL (1998): Basolateral amygdala noradrenergic influence on the memory-enhancing effect of glucocorticoid receptor activation in the hippocampus. Soc Neurosci Abstr 24:1901.
102. Roozendaal B., Portillo-Marquez G., McGaugh J.L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav Neurosci. 110:1996;1074-1083.
103. Roozendaal B., Williams C.L., McGaugh J.L. Glucocorticoid receptor activation of noradrenergic neurons within the rat nucleus of the solitary tract facilitates memory consolidation Involvement of the basolateral amygdala . Eur J Neurosci. 11:1999;1317-1323.
104. Sandi C., Loscertales M., Guanza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci. 9:1997;637-642.
105. Sandi C., Rose S.P.R. Corticosterone enhances long-term memory in one day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 647:1994;106-112.
106. Schultz J., Daly J.W. Accumulation of cyclic adenosine 3′,5′-monophosphate in cerebral cortical slices from rat and mouse Stimulatory effect of α- and β-adrenergic agents and adenosine . J Neurochem. 21:1973;1319-1326.
107. Setlow B, Roozendaal B, McGaugh JL (1998): Nucleus accumbens lesions block the memory-enhancing effects of immediate post-training systemic injections of dexamethasone. Soc Neurosci Abstr 24:174.
108. Starke K. Presynaptic regulation of catecholamines release in the central nervous system. Paton D.M. The Release of Catecholamines from Adrenergic Neurons. 1979;143-183 Pergamon Press, New York.
109. Stein L., Beluzzi J.D., Wise C.D. Memory enhancement by central administration of norepinephrine. Brain Res. 84:1975;329-335.
110. Sternberg D.B., Isaacs K., Gold P.E., McGaugh J.L. Epinephrine facilitation of appetitive learning Attenuation with adrenergic receptor antagonists . Behav Neural Biol. 44:1985;447-453.
111. Sternberg D.B., Korol D., Novack G., McGaugh J.L. Epinephrine-induced memory facilitation Attenuation by adrenergic receptor antagonists . Eur J Pharmacol. 129:1986;189-193.
112. Stone W.S., Croul C.E., Gold P.E. Attenuation of scopolamine-induced amnesia in mice. Psychopharmacology. 96:1988;417-420.
113. Tomaz C., Dickinson-Anson H., McGaugh J.L. Basolateral amygdala lesions block diazepam-induced anterograde amnesia in an inhibitory avoidance task. Proc Natl Acad Sci. 89:1992;3615-3619.
114. 2-agonist binding sites in the rat and human central nervous system analysis of some functional, anatomic correlates of the pharmacological effects of clonidine and related adrenergic agents . Brain Res. 319:1984;69-101.
115. Vazdarjanova A., McGaugh J.L. Basolateral amygdala is not a critical locus for memory of contextual fear conditioning. Proc Natl Acad Sci. 95:1998;15003-15007.
116. Vazdarjanova A, McGaugh JL (1999): Amygdala modulates consolidation of memory for classical conditioning. J Neurosci 19:6615-6622.
117. Wang S.J., Haung C.C., Hsu K.S., Tsai J.J., Gean P.W. Blockade of isoproterenol-induced synaptic potentiation by tetra-9-aminoacridine in the rat amygdala. Neurosci Lett. 214:1996;87-90.
118. Weiner N. Norepinephrine, epinephrine, and the sympathomimetic amines. Gilman G.L., Goodman L.S., Rall T.W., Murad F. The Pharmacological Basis of Therapeutics. 1985;145-180 Macmillan Publishing Company, New York.
119. Williams C.L., McGaugh J.L. Reversible inactivation of the nucleus of the tractus solitarius impairs retention performance in an inhibitory avoidance task. Behav Neural Biol. 58:1992;204-208.
120. Williams C.L., McGaugh J.L. Reversible lesions of the nucleus of the tractus solitarius attenuate the memory-modulatory effects of posttraining epinephrine. Behav Neurosci. 107:1993;1-8.
121. Williams C.L., Men D., Clayton E.C., Gold P.E. Norepinephrine release in the amygdala following systemic injection of norepinephrine or escapable footshock Contribution of the nucleus of the solitary tract . Behav Neurosci. 112:1998;1414-1422.
122. Williams C., Packard M.G., McGaugh J.L. Amphetamine facilitation of win-shift radial maze retention the involvement of peripheral adrenergic and central dopaminergic systems . Psychobiology. 22:1994;141-148.
123. Zilles K., Qu M., Schleicher A. Regional distribution and heterogeneity of α-adrenoceptors in the rat and human central nervous system. J fur Hirforshung. 2:1993;123-132.