Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation.

Previously, we reported that bilateral excitotoxic lesions of the basolateral nucleus of the amygdala (BLA) block the enhancing effects of posttraining systemic or intrahippocampal glucocorticoid administration on memory for inhibitory avoidance training. The present study further examined the basis of this permissive influence of the BLA on hippocampal memory functioning. Immediate posttraining unilateral infusions of the specific glucocorticoid receptor agonist RU 28362 (11beta,17beta-dihydroxy-6, 21-dimethyl-17alpha-pregna-4,6-trien-20-yn-3-one; 3.0, 10.0, or 30.0 ng in 0.5 microliter) administered into the dorsal hippocampus of male Sprague-Dawley rats induced dose-dependent enhancement of 48-h inhibitory avoidance retention. Infusions of the beta-adrenoceptor antagonist atenolol (0.5 microgram in 0.2 microliter) into the ipsilateral, but not the contralateral, BLA 10 min prior to training blocked the hippocampal glucocorticoid effects on memory consolidation. Infusions of the muscarinic cholinergic antagonist atropine (0.5 microgram in 0.2 microliter) into either the ipsilateral or contralateral BLA before training did not block the hippocampal glucocorticoid effects. These findings provide further evidence that beta-adrenergic activity in the BLA is essential in enabling glucocorticoid-induced modulation of memory consolidation and are consistent with the hypothesis that the BLA regulates the strength of memory consolidation in other brain structures. The ipsilateral nature of the BLA-hippocampus interaction indicates that BLA influences on hippocampal memory processes are mediated through neural pathways rather than by influences by means of the activation of peripheral stress responses.

[1]  J. D. McGaugh,et al.  Norepinephrine Release in the Amygdala in Response to Footshock Stimulation , 1996, Neurobiology of Learning and Memory.

[2]  J. D. McGaugh,et al.  Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Y. Ikegaya,et al.  High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo , 1995, Neuroscience Research.

[4]  Amygdaloid complex modulates neurotransmission from the entorhinal cortex to the dentate gyrus of the rat , 1984, Brain Research.

[5]  M. Gallagher,et al.  Memory formation: evidence for a specific neurochemical system in the amygdala. , 1977, Science.

[6]  J. D. McGaugh,et al.  Noradrenergic and cholinergic interactions in the amygdala and the modulation of memory storage , 1993, Behavioural Brain Research.

[7]  T. Shors,et al.  Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala , 1996, Neuroscience.

[8]  N. Spear,et al.  Neurobehavioral Plasticity : Learning, Development, and Response to Brain Insults , 1995 .

[9]  J. D. McGaugh,et al.  Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory , 1998, Neuroscience.

[10]  J. D. McGaugh,et al.  Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[12]  T. Di Paolo,et al.  Participation of the central amygdaloid nucleus in the response of adrenocorticotropin secretion to immobilization stress: opposing roles of the noradrenergic and dopaminergic systems. , 1987, Neuroendocrinology.

[13]  D. Diamond,et al.  Inverted‐U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation , 1992, Hippocampus.

[14]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[16]  J. D. McGaugh,et al.  Glucocorticoid Receptor Agonist and Antagonist Administration into the Basolateral but Not Central Amygdala Modulates Memory Storage , 1997, Neurobiology of Learning and Memory.

[17]  W Wippich,et al.  Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. , 1996, Life sciences.

[18]  P. E. Gold,et al.  Norepinephrine release in the amygdala after systemic injection of epinephrine or escapable footshock: contribution of the nucleus of the solitary tract. , 1998, Behavioral neuroscience.

[19]  Y. Ikegaya,et al.  Amygdala beta-noradrenergic influence on hippocampal long-term potentiation in vivo. , 1997, Neuroreport.

[20]  Y Watanabe,et al.  Effects of glucocorticoids on hippocampal long‐term potentiation , 1993, Hippocampus.

[21]  S. Nakajima,et al.  Effect of corticosteroids in the hippocampus on passive avoidance behavior in the rat , 1977, Pharmacology Biochemistry and Behavior.

[22]  Y. Ikegaya,et al.  Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats , 1994, Brain Research.

[23]  J. D. McGaugh,et al.  Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage , 1990, Brain Research.

[24]  J. D. McGaugh,et al.  Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs , 1998, Brain Research.

[25]  James L. McGaugh,et al.  Posttraining Intraamygdala Infusions of Oxotremorine and Propranolol Modulate Storage of Memory for Reductions in Reward Magnitude , 1997, Neurobiology of Learning and Memory.

[26]  Bruce S. McEwen,et al.  The acute effects of corticosteroids on cognition: integration of animal and human model studies , 1997, Brain Research Reviews.

[27]  James L. McGaugh,et al.  Stress and glucocorticoids impair retrieval of long-term spatial memory , 1998, Nature.

[28]  James L. McGaugh,et al.  Norepinephrine Infused into the Basolateral Amygdala Posttraining Enhances Retention in a Spatial Water Maze Task , 1999, Neurobiology of Learning and Memory.

[29]  T. Gray,et al.  Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. , 1991, Neuroendocrinology.

[30]  J. D. McGaugh,et al.  Basolateral Amygdala Lesions Block the Memory‐enhancing Effect of Glucocorticoid Administration in the Dorsal Hippocampus of Rats , 1997, The European journal of neuroscience.

[31]  B. McEwen,et al.  Selective Retention of Corticosterone by Limbic Structures in Rat Brain , 1968, Nature.

[32]  A. Pitkänen,et al.  Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat , 1999, The Journal of comparative neurology.

[33]  J L McGaugh,et al.  Basolateral Amygdala Is Involved in Modulating Consolidation of Memory for Classical Fear Conditioning , 1999, The Journal of Neuroscience.

[34]  J. D. McGaugh,et al.  Response of amygdalar norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC , 1999, Brain Research.

[35]  B. Roozendaal,et al.  Attenuated cardiovascular, neuroendocrine, and behavioral responses after a single footshock in central amygdaloid lesioned male rats , 1991, Physiology & Behavior.

[36]  J. Rothuizen,et al.  Binding characteristics of mineralocorticoid and glucocorticoid receptors in dog brain and pituitary. , 1990, Endocrinology.

[37]  L. Chen,et al.  The role of amygdala norepinephrine in memory formation: involvement in the memory enhancing effect of peripheral epinephrine. , 1995, The Chinese journal of physiology.

[38]  I. Izquierdo,et al.  Sequential Role of Hippocampus and Amygdala, Entorhinal Cortex and Parietal Cortex in Formation and Retrieval of Memory for Inhibitory Avoidance in Rats , 1997, The European journal of neuroscience.

[39]  A. Ohno,et al.  Role of Inhibition of Penicillin Binding Proteins and Cell Wall Cross-Linking by Beta-Lactam Antibiotics in Low- and High-Level Methicillin Resistance of Staphylococcus aureus , 1999, Chemotherapy.

[40]  J. Criado,et al.  Cholinergic responses of morphologically and electrophysiologically characterized neurons of the basolateral complex in rat amygdala slices , 1997, Neuroscience.

[41]  J. D. McGaugh,et al.  Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. , 1996, Behavioral neuroscience.

[42]  T. Shors,et al.  NMDA receptor antagonism in the lateral/basolateral but not central nucleus of the amygdala prevents the induction of facilitated learning in response to stress. , 1998, Learning & memory.

[43]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[44]  M. Joëls,et al.  Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems , 1994, Progress in Neurobiology.

[45]  P. Gean,et al.  Actions of isoproterenol on amygdalar neurons in vitro. , 1994, The Chinese journal of physiology.

[46]  R. Anwyl,et al.  Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. D. McGaugh,et al.  Effects of concurrent manipulations of cholinergic and noradrenergic function on learning and retention in mice , 1989, Brain Research.

[48]  J. Newcomer,et al.  Glucocorticoid-induced impairment in declarative memory performance in adult humans , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  J. D. McGaugh,et al.  Clenbuterol Administration into the Basolateral Amygdala Post-training Enhances Retention in an Inhibitory Avoidance Task , 1999, Neurobiology of Learning and Memory.

[50]  J. D. McGaugh,et al.  Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training , 1994, Brain Research.

[51]  C. Destrade,et al.  Time-dependent effects of posttraining intrahippocampal injections of corticosterone on retention of appetitive learning tasks in mice. , 1984, European journal of pharmacology.

[52]  L. Daws,et al.  Effects of Antidepressant Treatment on Inhibitory Avoidance Behavior and Amygdaloid β-Adrenoceptors in Rats , 1998, Neuropsychopharmacology.

[53]  E. R. Kloet,et al.  Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. , 1985, Endocrinology.

[54]  J. D. McGaugh,et al.  Memory-enhancing effects of posttraining naloxone: involvement of ß-noradrenergic influences in the amygdaloid complex , 1988, Brain Research.

[55]  K. Hsu,et al.  Blockade of isoproterenol-induced synaptic potentiation by tetra-9-aminoacridine in the rat amygdala , 1996, Neuroscience Letters.

[56]  A. McIntosh,et al.  Network interactions among limbic cortices, basal forebrain, and cerebellum differentiate a tone conditioned as a Pavlovian excitor or inhibitor: fluorodeoxyglucose mapping and covariance structural modeling. , 1994, Journal of neurophysiology.

[57]  T. Gray,et al.  The central amygdaloid nucleus innervation of the dorsal vagal complex in rat: A Phaseolus vulgaris leucoagglutinin lectin anterograde tracing study , 1989, Brain Research Bulletin.

[58]  Michael Davis,et al.  Neurotransmission in the rat amygdala related to fear and anxiety , 1994, Trends in Neurosciences.

[59]  K. Liang,et al.  Formation and retrieval of inhibitory avoidance memory: differential roles of glutamate receptors in the amygdala and medial prefrontal cortex. , 1996, The Chinese journal of physiology.

[60]  M. Packard,et al.  Amygdala Modulation of Multiple Memory Systems: Hippocampus and Caudate-Putamen , 1998, Neurobiology of Learning and Memory.

[61]  P. E. Gold,et al.  Intra-amygdala infusions of scopolamine impair performance on a conditioned place preference task but not a spatial radial maze task , 1998, Behavioural Brain Research.

[62]  F. H. Lopes da Silva,et al.  Electrophysiology of the Hippocampal and Amygdaloid Projections to the Nucleus Accumbens of the Rat: Convergence, Segregation, and Interaction of Inputs , 1998, The Journal of Neuroscience.

[63]  D. Geldmacher,et al.  The Amygdala , 1992, Neurology.

[64]  M. Witter,et al.  Entorhinal-Hippocampal Interactions Revealed by Real-Time Imaging , 1996, Science.

[65]  J. D. McGaugh,et al.  Amygdala β-Noradrenergic Influences on Memory Storage Involve Cholinergic Activation , 1996, Neurobiology of Learning and Memory.

[66]  Hyperpolarization-activated currents in neurons of the rat basolateral amygdala. , 1993, Journal of neurophysiology.

[67]  J. D. McGaugh,et al.  Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system , 1986, Brain Research.

[68]  J. Price,et al.  Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat , 1978, The Journal of comparative neurology.

[69]  James L. McGaugh,et al.  Basolateral Amygdala Noradrenergic Influences on Memory Storage Are Mediated by an Interaction between β- and α1-Adrenoceptors , 1999, The Journal of Neuroscience.

[70]  J. D. McGaugh,et al.  Involvement of the amygdala in memory storage: interaction with other brain systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  James L. McGaugh,et al.  Amygdaloid Nuclei Lesions Differentially Affect Glucocorticoid-Induced Memory Enhancement in an Inhibitory Avoidance Task , 1996, Neurobiology of Learning and Memory.

[72]  Joseph E LeDoux,et al.  Differential Effects of Amygdala Lesions on Early and Late Plastic Components of Auditory Cortex Spike Trains during Fear Conditioning , 1998, The Journal of Neuroscience.

[73]  E. D. de Kloet,et al.  Antiglucocorticoid RU 38486 attenuates retention of a behaviour and disinhibits the hypothalamic-pituitary adrenal axis at different brain sites. , 1988, Neuroendocrinology.

[74]  J. D. McGaugh,et al.  The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis , 1996, Brain Research.