From messengers to molecules, memories are made of these g riedel, b platt (kluwer, 2004)

NEUROSCIENCE INTELLIGENCE UNIT Gernot Riedel and Bettina Platt RIEDEL • PLATT NIU From Messengers to Molecules: Memories Are Made of These From Messengers to Molecules: Memories Are Made of These NEUROSCIENCE INTELLIGENCE UNIT From Messengers to Molecules: Memories Are Made of These Gernot Riedel, Ph.D Bettina Platt, Ph.D School of Medical Sciences College of Life Sciences and Medicine University of Aberdeen Foresterhill, Aberdeen, U.K LANDES BIOSCIENCE / EUREKAH.COM GEORGETOWN, TEXAS U.S.A KLUWER ACADEMIC / PLENUM PUBLISHERS NEW YORK, NEW YORK U.S.A FROM MESSENGERS TO MOLECULES: MEMORIES ARE MADE OF THESE Neuroscience Intelligence Unit Landes Bioscience / Eurekah.com Kluwer Academic / Plenum Publishers Copyright ©2004 Eurekah.com and Kluwer Academic / Plenum Publishers All rights reserved No part of this book may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system; for exclusive use by the Purchaser of the work Printed in the U.S.A Kluwer Academic / Plenum Publishers, 233 Spring Street, New York, New York, U.S.A 10013 http://www.wkap.nl/ Please address all inquiries to the Publishers: Landes Bioscience / Eurekah.com, 810 South Church Street Georgetown, Texas, U.S.A 78626 Phone: 512/ 863 7762; FAX: 512/ 863 0081 www.Eurekah.com www.landesbioscience.com From Messengers to Molecules: Memories Are Made of These, edited by Gernot Riedel and Bettina Platt, Landes / Kluwer dual imprint / Landes series: Neuroscience Intelligence Unit ISBN: 0-306-47862-5 While the authors, editors and publisher believe that drug selection and dosage and the specifications and usage of equipment and devices, as set forth in this book, are in accord with current recommendations and practice at the time of publication, they make no warranty, expressed or implied, with respect to material described in this book In view of the ongoing research, equipment development, changes in governmental regulations and the rapid accumulation of information relating to the biomedical sciences, the reader is urged to carefully review and evaluate the information provided herein Library of Congress Cataloging-in-Publication Data From messengers to molecules : memories are made of these / [edited by] Gernot Riedel, Bettina Platt p ; cm (Neuroscience intelligence unit) Includes bibliographical references and index ISBN 0-306-47862-5 Neurochemistry Neurotransmitters Neurotransmitter receptors I Riedel, Gernot II Platt, Bettina III Series: Neuroscience intelligence unit (Unnumbered) [DNLM: Memory physiology Ion Channels Learning physiology Memory Disorders Neurotransmitters Transcription Factors WL 102 F9308 2004] QP356.3.F76 2004 612.8'042 dc22 2004001884 Dedication To our children Daniel and Lisa Sophie, for wonderful memories CONTENTS Preface ix Abbreviations xxi Section Ions and Ion Channels 1.1 Calcium Miao-Kun Sun and Daniel L Alkon Ca2+ Influx Neurotransmitter Release Modulation of Channel Activity Signal Transduction Cascades Alzheimer’s Disease 14 1.2 Potassium 20 Jeffrey Vernon and Karl Peter Giese How Can K+ Channels Contribute to Learning and Memory? 22 Section Principle Neurotransmitters 2.1 Glutamate Receptors 39 Gernot Riedel, Jacques Micheau and Bettina Platt Glutamate Receptor Function in Learning and Memory Formation 43 2.2 γ-Amino-Butyric Acid (GABA) 72 Claudio Castellano, Vincenzo Cestari and Alessandro Ciamei GABAergic Drugs and Memory Formation: Peripheral Administrations 73 GABAergic Drugs and Memory: Genotype-Dependent Effects 75 GABAergic Drugs and the State-Dependency Hypothesis 76 GABAergic Drugs and Memory Formation: Administrations into Brain Structures 77 Interaction with Other Systems 82 2.3 Acetylcholine: I Muscarinic Receptors 90 Giancarlo Pepeu and Maria Grazia Giovannini Muscarinic Receptors 93 Which Cognitive Processes Depend on the Activation of Muscarinic Receptors? 98 Effects of Direct and Indirect Selective Muscarinic Receptor Agonists on Learning and Memory: Therapeutic Implications 103 2.4 Acetylcholine: II Nicotinic Receptors 113 Joyce Besheer and Rick A Bevins Neuronal nAChRs 113 Memory 115 Attention 117 Rewarding/Incentive Effects 118 Other Effects 120 2.5 Serotonin 125 Marie-Christine Buhot, Mathieu Wolff and Louis Segu Role of 5-HT in Memory: Global Strategies 126 Serotonergic-Cholinergic Interactions 128 5-HT Receptors in Memory Systems 128 2.6 Dopamine 143 Jan P.C de Bruin Functional Studies Using a Systemic Approach 145 Functional Studies Using a Central Approach 148 2.7 Adrenaline and Noradrenaline 155 Marie E Gibbs and Roger J Summers Pharmacology of α- and β-Adrenoceptors in the Central Nervous System 155 Factors Affecting Drug Action at Adrenoceptors 159 Memory Studies with Adrenoceptor Agonists and Antagonists in Rats 160 Memory Studies with Adrenoceptor Agonists and Antagonists in Chicks 163 Roles for Adrenoceptor Subtypes in the LPO 169 2.8 Histamine 174 Rüdiger U Hasenöhrl and Joseph P Huston The Histaminergic Neuron System 174 The Role of the Tuberomammillary Nucleus Projection System in Neural Plasticity and Functional Recovery 176 The Role of the Histaminergic Neuronal System in the Control of Reinforcement 178 The Role of the Histaminergic Neuronal System in the Control of Learning and Mnemonic Processes 181 Tuberomammillary Modulation of Hippocampal Signal Transfer 187 2.9 Adenosine and Purines 196 Trevor W Stone, M-R Nikbakht and E Martin O’Kane Origin of Adenosine in the Extracellular Fluid 196 Adenosine Receptors 196 Adenosine and Learning 197 Adenosine and Synaptic Plasticity 199 Interactions between Adenosine and Cholinergic Neurotransmission 201 Interactions between Purines and Glutamate Receptors 203 Other Receptor Interactions 205 The Effects of Ageing on Adenosine Receptors 210 Trophic Functions of Nucleosides 210 Nucleotides and Synaptic Plasticity 211 Section Neuromodulators 3.1 Cannabinoids 224 Lianne Robinson, Bettina Platt and Gernot Riedel Cannabinoid Receptors 224 Cannabinoid Receptor Ligands 225 Cannabinoid Receptors Modulate Memory Formation 226 3.2 Opioids 246 Makoto Ukai, Ken Kanematsu, Tsutomu Kameyama and Takayoshi Mamiya Distribution of Opioid Peptides and Their Receptors in the Hippocampus 246 Effects of Opioid Receptor Ligands on Long-Term Potentiation in Hippocampal Regions 249 Effects of Opioid Receptor Ligands on Learning and Memory in Hippocampal Regions 251 Effects of Opioid Receptor Ligands on Learning and Memory Tasks 251 Ameliorating Effects of Opioid Receptor Ligands on Models of Learning and Memory Impairment 251 3.3 Neuropeptides 256 David De Wied and Gábor L Kovács Posterior Pituitary Peptides (Vasopressin, Oxytocin) 256 ACTH/MSH and Opioid Peptides 261 Hypophyseotropic Peptides (CRF, Somatostatin) 263 Brain-Gut Peptides (CCK, Neuropeptide Y, Galanin) 266 Substance P 270 Natriuretic Peptides, Angiotensin 272 Amyloid Peptides 277 3.4 Nerve Growth Factors and Neurotrophins 286 Catherine Brandner Neurotrophin Expression and Regulation of Neurogenesis during Development 287 Neurotrophin Receptors 287 Nerve Growth Factor and the Basal Forebrain Cholinergic System 287 Behavioral Studies of NGF Administrations 289 Discussion 295 3.5 Eph Receptors and Their Ephrin Ligands in Neural Plasticity 300 Robert Gerlai The Promiscuous Family of Eph Receptors 300 Function of Eph Receptors in the Normal Brain: Role in Plasticity and Memory 302 Mechanisms Mediating Eph Action: The First Working Hypotheses 306 3.6 Corticosteroids 314 Carmen Sandi Glucocorticoid Hormones and Receptors 314 Role of Glucocorticoids on Memory Consolidation 317 Neural Mechanisms Involved in Glucocorticoid Actions on Memory Consolidation 321 Effects of Chronic Exposure to Elevated Glucocorticoid Levels on Cognitive and Neural Function 324 Section Second Messengers and Enzymes 4.1 Adenylyl Cyclases 330 Nicole Mons and Jean-Louis Guillou Adenylyl Cyclases and Memory Formation in Invertebrates 331 The Drosophila System 332 A Specific Role for Mammalian Adenylyl Cyclases in Learning and Memory Processes: Heterogeneity of Mammalian Adenylyl Cyclases 333 4.2 Phospholipases and Oxidases 349 Christian Hölscher Phospholipases 350 Arachidonic Acid (ArA), a Second Messenger 351 Release of ArA 352 Time Course of Release 352 Targets of ArA 352 ArA and Metabolites of ArA As Transmitters and ‘Retrograde Messengers’ in Synaptic Plasticity 353 Oxygenases That Are of Importance in Memory Formation 357 Cyclooxygenases 358 The Timing of Memory Formation 362 Defined Steps in Memory Formation 362 A Potential Role for Defined Time Windows of Messenger Systems in Memory Formation 363 4.3 Protein Kinase A 369 Monica R.M Vianna and Ivan Izquierdo Short- and Long-Term Memory 370 One-Trial Avoidance 372 The cAMP/PKA Signaling Pathway 372 PKA Involvement in Long-Term Memory Formation 373 PKA Involvement in Short-Term Memory Formation 375 PKA Involvement in Memory Retrieval 378 PKA Involvement in Extinction 379 4.4 Protein Kinase C 383 Xavier Noguès, Alessia Pascale, Jacques Micheau and Fiorenzo Battaini Protein Kinase C: Who Is It? 384 PKC in Synaptic Plasticity 386 Evidence for the Involvement of PKC in Cognitive Processes 389 PKC and Neuronal Pathologies Impairing Cognition 395 Pharmacological Modulation of PKC: The Goal of Isoenzyme Selectivity 400 4.5 CaMKinase II 411 Martín Cammarota and Jorge H Medina CaMKII: Synaptic Plasticity and Memory Processing 412 Downstream Effectors of the CaMKII Cascade 416 CaMKIV: A New (and Important) Player in the Plasticity Team 418 4.6 MAP Kinases 425 Joel C Selcher, Edwin J Weeber and J David Sweatt Hippocampal Involvement in Learning 429 ERK in Hippocampal Synaptic Plasticity 433 A Necessity for ERK Activation for Mammalian Learning 435 Specific Contributions of ERK Isoforms to LTP and Learning 440 Biochemical Attributes That Make ERK Suited for Memory Formation 442 4.7 Phosphatases 448 Pauleen C Bennett and Kim T Ng Phosphorylation in Information Storage Processes 458 Phosphatase Involvement in Invertebrate Memory Models 462 Protein Phosphatases in Aplysia Learning and Memory 463 Phosphorylation in Vertebrate Memory Models 464 4.8 Nitric Oxide 480 Kiyofumi Yamada and Toshitaka Nabeshima Regulation of NO Synthesis in the Brain 480 Role of NO in LTP and LTD 481 Role of NO in Memory Processes 483 Learning and Memory-Associated Changes in NO Production in the Brain 487 Section Transcription Factors, Genes and Proteins 5.1 CREB 492 Paul W Frankland and Sheena A Josselyn Structure 493 Activation 493 CREB and Electrophysiological Studies of Long-Term Plasticity in Aplysia 495 CREB and Memory in Drosophila 496 CREB and LTM in Mammals 496 Gaining Temporal and Spatial Control of CREB Function in Mammals 497 5.2 Immediate-Early Genes 506 Jeffrey Greenwood, Pauline Curtis, Barbara Logan, Wickliffe Abraham and Mike Dragunow Learning Activates IEGs 507 A Link between Cholinergic System and IEGs 507 IEGs and Their Relation to Stress 508 5.3 Protein Synthesis: I Pharmacology 514 Oliver Stork and Hans Welzl Asking about the ‘Where’ and ‘When’ of Learning-Related Protein Synthesis 514 Inhibitors of Protein Synthesis 516 Effects of Protein Synthesis Inhibitors on Memory Formation 519 Principle Findings and Future Perspectives in Protein Synthesis Inhibitor Research 522 5.4 Protein Synthesis: II New Proteins 529 Radmila Mileusnic Present Time 533 Section Morphological Changes in Synapses and Neurones 6.1 Learning-Induced Synaptogenesis and Structural Synaptic Remodeling 543 Yuri Geinisman, Robert W Berry and Olga T Ganeshina Patterns of Synaptogenesis Elicited by Behavioral Learning 543 Specific Synaptogenesis Related to Learning-Induced Adult Neurogenesis 547 Pattern of Structural Synaptic Remodeling Elicited by Behavioral Learning 553 Enlargement of Postsynaptic Densities following Learning: A Possible Morphological Correlate of the Conversion of Postsynaptically Silent Synapses into Functional Synapses 556 600 From Messengers to Molecules: Memories Are Made of These opment, survival, and plasticity.23,126 The route of Ca2+ entry determines which signaling pathways are activated, and thus plays a critical role in specifying the cellular response to Ca2+ For example, L-type Ca2+ influx is particularly effective in activating transcription factors such as CREB and MEF-2.23 Given the numerous changes in the Ca2+ signaling mechanisms in aging, it is conceivable that the profile of gene expression alters with age as well As the sIAHP is a compensatory mechanism to counter neuronal Ca2+ overload, it is possible that the functional channel density for the sIAHP channels is upregulated in aging sIAHP As a Link Between Age-Related Changes in Ca2+ Homeostasis and Learning Depending on the route of entry, Ca2+ can differentially modulate the sIAHP by activating different kinase cascades and affecting subsequent plastic changes The interaction between the Ca2+ signaling cascade and the glutamatergic system exemplifies the complex nature of the regulation of the sIAHP and neuronal excitability In hippocampal pyramidal neurons, NMDAR-mediated Ca2+ influx can activate the sIAHP in the absence of action potentials.51 However at synapses, this Ca2+ influx shows associative features in that it becomes supralinear when it occurs with the pairing of an action potential and EPSPs.43,129,130 Likewise, repetitive activation of mGluRs can induce large increases in intracellular Ca2+ level at the proximal dendrite when paired with backpropagating action potentials.74 Given the putative locations of the sIAHP channels,9,11,97 the NMDA receptor- and mGluR-mediated Ca2+ transients might be especially important in regulating the sIAHP by strategically increasing local dendritic Ca2+ levels and activating local kinase cascades Furthermore, in hippocampal pyramidal neurons, the Ca2+ transient evoked by stronger stimulation is dependent on VGCCs but independent of NMDAR, whereas the Ca2+ transient evoked by subthreshold stimulation is independent of voltage-gated Ca2+ channels and dependent on NMDA receptors Thus, differential modulation of the sIAHP by Ca2+ channels and the glutamatergic system can be adjusted in an activity-dependent manner The exact biochemical steps that lead to changes in the sIAHP in learning hippocampus-dependent tasks and in aging are not totally understood What is clear, however, is that numerous neuromodulators can alter both sIAHP and higher brain functions For example, activation of mGluRs has been shown to reduce the AHP and the sIAHP.1,13,16,20,59 However, by activating PKC, mGluRs can also prevent activation of β-adrenergic receptors, which couple to adenylyl cyclase, from blocking the sIAHP.76 Since the AHP modulates neuronal responsiveness, cross talk between PKC and the adenylyl cyclase pathway is likely to have physiological consequences The interference with the β-adrenergic response by mGluRs suggests that under physiological conditions, mGluRs can exert dominance over β-adrenergic receptors in a task-specific manner Furthermore, it is likely that these mechanisms also involve Ca2+ signaling and second messenger systems that were previously implicated in other forms of synaptic plasticity For example, kinases known to modulate the sIAHP—PKC, PKA, and CaMKII—are also important for the induction of LTP Pharmacological manipulations that facilitated LTP have also been shown to reduce the AHP,16 suggesting that the AHP and its underlying currents can serve as an adjustable gain control, variably hyperpolarizing and shunting synaptic potentials arising in the apical dendrites and controlling the induction of LTP.97 A recent study confirmed this hypothesis, demonstrating that steady state activation of the sIAHP dampens temporal summation of the EPSPs as well as speeds 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Hasselmo ME The hippocampus as an associator of discontiguous events Trends Neurosci 1998; 21:317-323 124 Weiss C, Bouwmeester H, Power JM et al Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat Behav Brain Res 1999; 99:123-132 125 Weiss C, Preston AR, Oh MM et al The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons J Neurosci 2000; 20:783-790 126 West AE, Chen WG, Dalva MB et al Calcium regulation of neuronal gene expression Proc Natl Acad Sci 2001; 98:11024-11031 127 Wu WW, Disterhoft JF Calcium homeostasis and learning deficits in ageing In: Mattson M, ed Advances in Cell Aging and Gerontology New York: Elsevier, 2002 128 Wu WW, Oh MM, Disterhoft JF Age-related biophysical alterations of hippocampal pyramidal neurons: Implications for learning and memory Ageing Res Rev 2002; 1:181-207 129 Yuste R, Majewska A, Cash SS et al Mechanisms of calcium influx into hippocampal spines: Heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis J Neurosci 1999; 19:1976-1987 130 Yuste R, Majewska A, Holthoff K From form to function: Calcium compartmentalization in dendritic spines Nature Neurosci 2000; 3:653-659 131 Zhang L, Pennefather P, Velumian A et al Potentiation of a slow Ca(2+)-dependent K+ current by intracellular Ca2+ chelators in hippocampal CA1 neurons of rat brain slices J Neurophysiol 1995; 74:2225-2241 Index A α-adrenoceptor 155 Accommodation 594-597 Acetylcholine (ACh) 3, 14, 22, 29, 74, 83, 90-100, 102-104, 113, 114, 119, 125, 126, 128, 132-137, 181, 186, 196, 198, 201-205, 210, 220, 221, 223, 225, 230, 238, 254, 258, 260, 261, 265, 266, 269-273, 277, 283, 351, 354, 446, 506, 507, 580-582, 592 Actinomycin-D 418, 514, 516, 517, 521, 530, 531 Activating transcription factor (ATF-1) 415, 418, 493 Activating transcription factor (ATF3) 508-511 Adenosine 3, 189, 196-205, 207, 210-212, 214, 277, 330, 333, 449, 456, 492 Adenylate cyclases 26-28, 144, 156-158, 224, 260, 265, 270, 330, 331, 333, 336, 337, 339, 340, 372, 374, 419, 455, 459, 461, 463, 493, 495, 496, 600 Adrenaline 155, 159, 161, 317 Adreno-receptors 155, 164 Adrenocorticotropin (ACTH) 76, 258, 261, 263, 273, 274, 277-279, 314, 315, 414 Affective disorder 400, 410 Afterhyperpolarisation (AHP) 8, 20, 22, 25, 29, 30, 134, 591, 592, 594-598, 600 Aging 1, 2, 33, 39, 90, 96, 97, 117, 125, 134, 135, 137, 182, 210, 265, 295, 325, 406, 408-410, 431, 480, 488, 547, 559, 591-596, 598-600 Alzheimer’s disease (AD) 12, 14, 29, 90-93, 96, 97, 103, 113, 116, 125, 128, 134, 135, 137, 182, 189, 201, 269, 277, 351, 397, 398, 467, 506, 507, 511, 580 Amnesia (animal and human) 580 AMPA 4, 39-41, 43, 49-52, 54-56, 59, 61, 70, 71, 80, 200, 205, 259, 309, 352, 356, 375, 378, 414-417, 431, 432, 447, 459, 462, 493, 534, 554, 556, 557, 559, 592, 598 Amphetamine 146, 161, 262, 274, 531, 532 Amygdala 49, 51, 52, 59, 61, 72, 76-81, 83-85, 89, 92, 93, 95, 96, 101, 114, 127, 128, 133, 144, 155, 158, 160-162, 165, 170, 171, 174, 176, 226, 239, 258, 263, 267, 268, 271-276, 301, 314, 316, 317, 321, 323, 326, 338, 372, 378, 379, 386, 388, 390-392, 416, 433, 447, 498-500, 516, 521, 522, 534, 580 Amyloid 3, 12, 14, 97, 252, 277, 278, 351, 397, 398, 506 Amyotrophic lateral sclerosis (ALS) 399 Anandamide 225, 232, 233, 235, 236, 239-241 Angiotensin (Ang) 272-277, 279 Anticonvulsant 197 Apis 28, 520 Aplysia 22, 23, 25, 26, 31, 32, 33, 330-332, 347, 354, 358, 361, 370, 389, 427, 430, 433, 448, 462-464, 493, 495, 496, 500, 501, 518, 519, 569, 574, 576 Arachidonic acid (ArA) 3, 10, 13, 129, 225, 234, 349, 351-364 Arousal 91, 102, 132, 155, 169, 175, 180, 259, 261-265, 279, 452 Associative learning 8-11, 20, 26-28, 96, 98, 119, 135, 136, 264, 331, 332, 436, 443, 500, 548, 557, 575, 594 Attention 1, 15, 25, 29, 61, 90, 91, 98, 101, 102, 113, 115, 117-121, 135, 136, 143, 144, 149, 162, 169, 174, 196, 197, 238, 242, 259, 261, 263, 264, 268, 279, 290, 295, 296, 300, 314, 321, 322, 325, 331, 386, 388, 398, 420, 430, 451, 462, 464, 519, 532, 535 Attention deficit disorder 113 Autophosphorylation 287, 301, 304, 310, 337, 385, 411-417, 456, 461, 464 Axospinous synapse 543, 545, 547, 550, 553-557, 559, 575 608 From Messengers to Molecules: Memories Are Made of These B β-adrenoceptor 155, 156, 158, 159 Baclofen 72, 75, 76, 78, 204, 205 Basal forebrain 79, 92-94, 96, 97, 100, 102, 115, 131, 174, 175, 180, 252, 270, 272, 277, 286-289, 295, 506, 580 Benzodiazepine 43, 72, 84 Bicuculline 73-79, 81-85, 200, 204, 205, 273 Brain-derived neurotrophic factor (BDNF) 259, 265, 287, 289, 494, 295, 300, 418, 494, 495, 514, 523 C C elegans 28 Ca2+ (calcium) 1-15, 22, 25-30, 33, 41, 43, 49, 76, 93-95, 98, 129, 156, 157, 199-204, 211, 224, 249, 260, 265, 320, 330-343, 349-357, 361, 362, 369, 372, 384-388, 394, 396, 397, 399, 401, 403, 411-419, 427-432, 448, 449, 451, 454-457, 459-464, 470, 480-482, 487, 493-496, 508, 511, 518, 536, 554, 565, 566, 567, 570, 587, 591-596, 598-600 Ca2+ channel blockers 30, 199, 594 Ca2+ homeostasis 1, 2, 6, 7, 10-15, 591, 592, 594, 600 Ca2+ hypothesis 591 Ca2+-binding enzyme CA3 3, 4, 29, 98, 202, 233, 239, 247, 249-251, 257, 262, 263, 270, 325, 326, 336, 339, 363, 374, 388-391, 393, 394, 396, 403, 459, 547, 570, 595, 598 Cadherin 566, 567, 574, 576, 578, 579 Calcineurin 333, 335-337, 339, 432, 448, 451, 454, 494, 522 Calcium/calmodulin-dependent kinase (CaMK) 335, 419, 454, 459, 461, 462, 465, 470 CaMKII 6, 8, 9, 25, 27, 28, 32, 259, 335-337, 339, 351, 374, 379, 411-420, 432, 495, 523, 598, 600 CaMKIV 336, 418-420, 493, 495 Calmodulin 2, 4-6, 9, 27, 259, 331, 362, 369, 372, 387, 411, 412, 415, 418, 432, 455, 459, 480, 495, 587, 598 cAMP-dependent protein kinase see PKA Cannabinoids 224, 225, 226, 238-242, 333, 361 Cell adhesion molecules (CAM) 158, 322, 323, 363, 565-570, 572-577, 579 cGMP 5, 6, 156, 336, 480, 481, 482, 483, 485, 487, 488 cGMP-dependent protein kinase see PKG Chicks 54, 55, 57, 155, 160, 163-170, 277, 314, 318, 320-323, 349, 355-357, 359, 361-364, 374, 391, 392, 413, 448, 465-471, 485, 486, 520, 523, 534-536, 544, 545, 566, 573-576, 578, 579 Chloride channel 199 Cholecystokinin (CCK) 225-268, 274, 277-279 Cholinergic hypothesis 580, 583 Cholinergic system 83, 90-92, 96, 98-100, 102, 103, 113, 115-117, 128, 134, 181, 201, 240, 254, 260, 286, 287, 289, 295, 296, 397, 485, 506, 507, 581, 583 Cholinesterase inhibitors 30, 99, 103, 132, 506, 583 c-Jun 427, 508, 511, 523, 536 Cognitive demand 125, 135, 137 Coincidence detector 330, 331, 333-335, 337, 343, 425 Complexity 15, 125, 182, 431, 433, 458, 462, 495, 522, 535, 547, 583 Conditioning 23-32, 51, 53, 54, 59, 61, 75, 78, 79, 95, 96, 98, 99, 113, 128, 133, 146, 151, 152, 181, 182, 187-189, 232, 239, 241, 256, 264, 267, 268, 304-307, 317-319, 323, 326, 330, 332, 340, 361, 373, 374, 378, 379, 388-390, 392, 393, 401, 413, 416, 430, 431, 433, 435, 436, 439-441, 443, 464, 471, 483-485, 487, 496-498, 500, 516, 519-522, 544, 545, 548, 550, 553, 554, 556-559, 566, 567, 569, 572, 573, 577, 579, 586, 592, 594-597 Consolidation 22, 25, 29, 30, 39, 49, 51, 54, 55, 59, 61, 72, 73, 75-77, 79-83, 85, 95, 100, 116, 117, 126, 133-135, 155, 161-171, 182, 186, 226, 228-237, 240-242, 246, 256-259, 262-266, 269, 272, 273, 279, 305, 309, 314, 317-323, 332, 339, 349, 352, 355, 361-364, 369, 370, 372-375, 378, 379, 413, 414, 417-419, 432, 452, 455, 465, 471, 485, 498, 500, 507, 511, 521-523, 529-535, 538, 543, 545, 546, 558, 559, 564, 566-570, 572-578, 582, 595 609 Index Corticosteroid 314-320, 323, 324 Corticotropin-releasing factor (CRF) 263-265, 273, 274, 277, 279, 598 CREB 315, 331, 332, 338-340, 369, 370, 371, 373-375, 379, 415, 417-419, 427, 429, 463, 481, 492-498, 500, 501, 507, 508, 514, 523, 535, 539, 600 Cyclic adenosine monophosphate (cAMP) 6, 25-28, 41, 43, 50, 94, 98, 129, 134, 156-158, 207, 265, 266, 287, 315, 330-333, 335-340, 342, 343, 358, 369, 370, 372-375, 379, 416, 418, 419, 426, 427, 456, 457, 462-464, 492, 493, 495, 496, 532, 598 Cycloheximide 252, 514, 517, 530, 531, 533, 578 Cyclooxygenase (COX) 349, 354, 357-364 D ∆9THC 224-226, 228-234, 236, 238-241 Development 1, 14, 26, 33, 39, 43, 95, 100, 102, 121, 137, 145, 148, 149, 156, 163, 201, 210, 224, 261, 266, 277, 286-289, 295, 296, 300-302, 309, 310, 322, 326, 351, 361, 362, 432, 440, 441, 451, 458, 461, 465, 469, 497, 498, 500, 514, 515, 532, 533, 553, 565, 570, 573-576, 579, 587, 599 Dihydropyridine 2, 3, Dopamine 11, 118-120, 143-145, 147, 148, 152, 177, 178, 186, 198, 205, 207, 212, 225, 230, 235, 266, 268, 270, 272-275, 339, 361, 378, 456, 598 Drosophila 21, 23, 26-28, 32, 33, 330-333, 373, 389, 417, 427, 436, 462, 464, 493, 496, 498, 501, 520, 567, 576 Dynorphin 247, 249-254, 262 E Eag 22, 25-28, 32 Eating behaviour 155 Encoding 2, 22, 25, 33, 39, 49, 54, 59, 80, 90, 93, 99, 103, 104, 115-117, 226, 239-242, 259, 264, 278, 302, 319, 336, 343, 414, 498, 500, 511, 534, 539, 570, 583, 586 Endocannabinoid 224, 225, 239-242 Endorphin 76, 83, 251, 253, 258, 262, 267, 274, 277, 279, 414 Endothelium-derived relaxing factor (EDRF) 480 Enzyme 1, 3, 9, 10, 13, 43, 61, 93, 98, 103, 114, 127, 129, 156, 174, 196, 214, 225, 288, 349-351, 353, 355, 357-359, 362, 364, 372, 374, 378, 379, 383-385, 390, 397, 401, 411, 412, 416, 418, 419, 442, 448-456, 458, 461-467, 469, 480, 492, 496, 514, 516, 572, 591 Eph receptor 300-302, 305, 306, 309, 310 Ephrin ligand 300-302, 306, 309, 310 EphrinA 301, 302, 304-306, 309, 310 EphrinB 301, 302, 306, 310 EPSPs 429 Ethanol 72, 84, 85 Excitability 1, 20, 22, 25-27, 30, 32, 33, 43, 50, 59, 94, 126, 134, 187, 196, 200, 201, 204, 205, 278, 279, 316, 352, 386, 425, 427, 544, 592, 594-598, 600 Extinction 25, 52-54, 74, 119, 128, 224, 232, 239, 257-259, 261, 262, 265, 266, 272-274, 369, 372, 379, 521, 522, 534 Extracellular signal-regulated kinase (ERK) 335, 336, 338, 343, 415, 417-419, 425-429, 433-437, 439-443, 493-495 F Fear conditioning 436 Fear memory 51, 516, 521-523 Flexibility 30, 134, 143, 149-151, 226, 326, 576, 584 Forgetting 198, 224, 226, 239, 241, 349, 364 G γ-amino-butyric acid (GABA) 8, 11, 59, 72, 76, 81-85, 95, 189, 198, 200, 225, 266, 269, 338, 356, 460 GABAA receptor 72, 73, 75, 76, 83, 85 GABAB receptor 72, 75, 76 GABAergic drug 72, 73, 75-77, 79, 83, 85 Galanin 252, 266, 269, 270, 274, 277 GAP-43 386-388, 466, 535, 537 Glucocorticoid 314, 315, 317-326, 379, 519, 523 Glutamate receptor 4, 11, 39-41, 43, 45, 49, 50, 53, 57, 61, 118, 196, 203-205, 351, 352, 378, 388, 459, 460, 481, 534, 536, 598 Glycosylation 532, 570, 572 610 From Messengers to Molecules: Memories Are Made of These H 8-HO-DPAT 374 5-HT 125, 126, 127, 128, 129, 130, 131, 132, 133, 134, 135, 136, 137, 270, 331, 332, 463, 477, 479 Hippocampus 434 Histamine 174-178, 180-182, 185-187, 189, 361, 598 Histaminergic neuronal system 174-176, 178, 181, 182, 189 Hormones 76, 104, 210, 260, 263, 264, 273, 274, 314-318, 320, 330, 333, 384, 414, 531, 532 HPA axis 265, 314, 316 Human amnesia 580 Huntington’s disease (HD) 399 Hypothalamus 92, 114, 115, 158, 159, 174-176, 178-180, 185, 258, 263, 265, 271, 273, 301, 314-316, 570 Hypothalamus-pituitary-adrenocortical (HPA) 264, 265, 314, 316 Hypoxia 2, 12, 13, 203, 569 I 192IgG-saporin 100, 101, 102 IMHV 57, 59, 165-170, 355, 392, 413, 537, 545 Immediate-early gene (IEG) 506-508, 511, 534-536, 538 Incentive salience 113, 119, 120 Inducible transgenic mice 515 Integrin 566, 567, 569, 574-578 Intracellular Ca2+ store 4, 6, 7, 260, 349, 592 IP3 receptor 5, 592 K K+ (potassium) 8, 12-14, 20-23, 25-33, 41, 76, 93-95, 129, 156, 199, 201, 202, 207, 211, 224, 260, 265, 354, 357, 399, 427-429, 433, 442, 463, 464, 594, 595, 598 K+ channel 8, 14, 20-23, 25-33, 93, 95, 156, 199, 201, 207, 224, 354, 357, 399, 427, 428, 433, 463 K+ current 20-22, 25-28, 31, 32, 94, 129, 207, 265, 427-429, 463, 464, 594, 595, 598 Kinase 1, 3, 5, 6, 9, 10, 13, 20, 22, 24-26, 28, 31, 32, 43, 98, 129, 157, 158, 196, 207, 214, 224, 259, 266, 286, 287, 300-302, 304, 309, 310, 330-333, 335, 336, 338, 351, 353, 362, 364, 369, 370, 372, 375, 383-388, 392, 395, 399-401, 411-419, 425-428, 431, 432, 435, 442, 443, 448-451, 453-456, 458-461, 464-466, 471, 481, 482, 493-495, 500, 501, 507, 508, 517, 519, 535, 536, 566, 568, 575, 576, 579, 598-600 Kvβ1.1 null mutant 29, 30, 33 L L1 309, 322, 323, 537, 567, 569, 573-579 Learning-induced synaptogenesis 543, 546 Lipoxygenase 349, 352, 355, 357, 358, 360, 361, 364 Lobus parolfactorius (LPO) 165-167, 169, 170, 413, 520, 545, 566, 576 Locomotor activity 95, 120, 125, 143, 145-147, 198, 238, 263, 264, 266, 269, 274, 275, 518, 519 Long term depression (LTD) 10, 11, 199, 200, 203, 246, 320, 355, 388, 430, 431, 433, 443, 458, 460-462, 471, 480-483, 487, 522, 582 Long-term memory (LTM) 13, 49, 51, 78, 80, 81, 99, 126, 128, 134, 158, 160, 163, 166, 210, 271, 276, 314, 317, 321, 323, 330-332, 338-340, 349, 362, 364, 369, 370, 372-375, 377-379, 391, 412-414, 419, 427, 429, 430, 452, 465, 471, 485, 492, 493, 495-498, 500, 501, 506, 507, 511, 514, 515, 518-523, 529-532, 534, 537-539, 543, 546, 564, 566, 568, 574 Long-term potentiation (LTP) 10, 11, 20, 22, 29-32, 95, 98, 118, 120, 135-137, 161, 196, 199, 200, 203-205, 212-214, 246, 249-251, 254, 258, 262, 263, 265, 267, 273, 276-278, 295, 300, 304, 305, 309, 320, 331, 336-340, 351-353, 355, 356, 358, 361, 362, 370, 374, 375, 386-388, 395, 412-414, 416-419, 425, 427-437, 439-441, 443, 448, 458-462, 466, 470, 471, 480-483, 487, 507-511, 522, 535-538, 550, 553-556, 559, 565, 567, 569, 570, 572, 574-579, 582, 600 Index M MAP2 (microtubule associated protein) 337, 450, 460, 523 MAPK see Mitogen-activated protein kinase Marijuana 224, 226 MEK 417, 418, 425-428, 434, 435, 437, 439, 494, 495, 507 Memory dysfunction 96, 580, 581 Mesocortical dopaminergic 143, 144, 147, 151 Mesocortical system 144 Mesolimbic dopaminergic 144, 146 Mesolimbic system 144 Metaplasticity 61, 383, 388, 394, 395, 402 mGlu 39, 43, 49-52, 54, 55, 59, 61 mGlu receptor (mGluR) 4, 11, 43, 49-52, 54, 55, 59, 61, 351-353, 355, 356, 375, 378, 388, 598, 600 Mineralocorticoid 314, 315, 317, 318 Mitogen-activated protein kinase (MAPK) 31, 98, 157, 158, 224, 259, 332, 333, 335, 336, 338, 370, 372, 378, 379, 417, 425, 426, 433, 435, 436, 440-443, 494, 517, 519, 521, 523 Mossy fiber 247, 249-251, 262, 302, 325, 337, 339, 388, 570, 547, 575 Motor activity 95, 102, 120, 125, 143, 145-147, 197, 198, 238, 263, 264, 266, 269, 274, 275, 394, 395, 402, 403, 518, 519, 574 MSH 261, 274, 277-279 Multiple-synapse bouton 543, 548, 550, 554, 558 Muscarinic receptor 90, 91, 93, 94, 96-99, 103, 104, 132, 201, 254, 286, 289, 506, 507, 598 Muscimol 72, 74-85, 582 N N-methyl-D-aspartate (NMDA) 2, 4, 8, 11, 29, 39-41, 43, 49-56, 59, 61, 85, 94, 98, 118, 132, 198, 200, 203-206, 212, 258, 259, 265, 275, 278, 309, 332, 337, 339, 351, 352, 354, 356-358, 364, 372, 373, 375, 378, 379, 387, 388, 412, 414-418, 429-433, 435, 442, 459, 460, 462, 480-482, 493, 507, 510, 511, 533, 536, 538, 554, 556, 557, 565, 572, 574, 577, 582, 586, 592, 594, 598, 600 Naloxone 82, 83, 161, 246, 249-251, 253, 273 611 Natriuretic peptides 272, 279 ANP 272, 274, 277 BNP 272, 274, 277 CNP 272-274, 277 NCAM 322, 323, 514, 537, 539, 567, 569-578 Nerve growth factor (NGF) 100, 259, 286-290, 292, 293, 295, 296, 300, 419, 494, 495, 586 Neural plasticity 118, 174, 176, 178, 286, 287, 300, 305, 309, 522 Neurexins 566, 567 Neurogenesis 127, 176, 287, 302, 543, 547, 548, 558, 572, 577-579 Neuroleptics 146, 176, 262 Neuromodulator 22, 78, 84, 174, 225, 254, 598, 600 Neuropeptides 189, 210, 256-258, 260-269, 271, 274, 277-280, 361, 598 Neuropeptide Y (NPY) 266, 268, 269, 274, 277, 279 Neurotransmitter 1, 3, 4, 7, 10, 11, 22, 25, 26, 29, 31, 39, 72, 73, 76, 77, 83, 84, 91, 95, 125, 128, 130-132, 134, 137, 143, 147, 152, 155, 171, 174, 196, 198, 200, 205, 210, 211, 214, 225, 246, 254, 256, 258, 269, 270, 273, 288, 309, 314, 315, 330, 333, 337, 349, 354, 361, 374, 375, 384, 411, 427, 431, 442, 449, 459, 460, 463, 482, 495, 506, 507, 529, 530, 538, 554, 556, 572, 580, 591, 598 Neurotrophic factor 265, 287, 295, 300, 302, 324, 494, 514, 523, 586 Neurotrophin 286-289, 296, 300 New proteins 369, 373, 449, 492, 514, 529, 530 Nicotine 76, 113, 115-120, 136 Nicotinic receptor 99, 113, 115, 117, 118 Nitric oxide (NO) 12, 13, 207, 231, 258, 273, 332, 354, 355, 361-364, 431, 455, 459, 480-487, 488, 574 Nitric oxide synthase (NOS) 12, 207, 273, 361, 362, 459, 480-488, 574 Noradrenaline 143, 155, 156, 159-163, 165, 166, 169-171, 198, 230, 231, 258, 261, 263, 265, 270, 317, 354, 452, 598 Nucleotide 22, 129, 144, 156, 196, 203, 211, 212, 265, 336, 426, 427, 436, 494 Nucleus accumbens 49, 51, 59, 95, 114, 118, 120, 127, 130, 143-146, 148, 149, 175, 176, 180, 185, 186, 196, 268, 271, 272, 275 612 From Messengers to Molecules: Memories Are Made of These O 6-OHDA 148, 176, 178, 189, 258, 265, 267, 273, 275 Odor discrimination 28, 59, 520, 569, 572, 575, 595 OLETF rat 267 Opioid 72, 76, 82, 83, 178, 246, 247, 249-254, 261, 262, 267, 271 Opioid receptor 246, 247, 249-254, 262 Oxidase 160, 349, 360, 362 Oxytocin 256-260, 273, 274, 277, 278 P p75NTR 286-289, 295, 296 Paired-pulse inhibition 200, 201, 204, 205 Parkinson’s disease 93, 99, 144, 189, 399 Perceptual processing 90, 104 Perforated synapse 550, 553, 554, 556, 559, 565 Pharmacology 93, 99, 130, 137, 155, 157, 175, 197, 211, 225, 246, 383, 514 Phosphatase 20, 310, 331, 333, 335, 337, 386, 414, 416, 432, 448-456, 458-466, 470, 471, 494, 576, 598, 599 Phospholipase 13, 43, 93, 97, 98, 129, 135, 156, 157, 260, 349-353, 355-358, 362, 384 Phospholipase C (PLC) 41, 43, 83, 97, 98, 129, 135, 152, 156, 157, 260, 350-353, 355, 356, 364 Phospholipase type A2 (PLA2) 129, 350, 351, 352, 355, 356, 364 Phosphorylate 426, 429 Phosphorylation 6, 8, 11-14, 20, 22, 28, 32, 98, 156-158, 214, 287, 301, 304, 309, 310, 330, 333, 335-339, 353, 354, 370, 375, 378, 384-388, 411-419, 426-429, 437, 442, 448-450, 452-466, 471, 481, 492-496, 500, 501, 506, 507, 514, 518, 519, 532, 535, 572, 598, 599 Picrotoxin 28, 72-79, 81-83, 85, 531 Pituitary 28, 256, 260, 263, 264, 273, 278, 279, 314-316 PKA (cAMP-dependent protein kinase, protein kinase A) 6, 25-28, 31, 32, 98, 158, 330-333, 335-340, 351, 369-379, 414, 417-419, 426, 428, 442, 453, 456, 457, 459-465, 470, 493, 495, 500, 519, 521-523, 598, 600 PKC (protein kinase C) 3, 6, 9, 10, 24-26, 31, 32, 41, 43, 98, 129, 156, 157, 207, 214, 259, 266, 330, 332, 333, 335-337, 351, 353, 354, 358, 362, 369, 370, 374, 383-404, 414, 416, 417, 426, 428, 432, 442, 455, 459, 463, 465, 466, 493, 570, 575, 579, 598, 600 PKG (cGMP-dependent protein kinase) 6, 453, 459, 465, 481, 482 Place preference 146, 178, 180, 186 Polysialic acid 323, 570, 574-579 Polysialylation (PSA) 323, 570-573, 575, 577 Postsynaptic density (PSD) 337, 412, 414-417, 433, 461, 543, 550, 553-557, 559, 565, 566, 575, 576 PP1 (protein phosphatase 1) 337, 339, 414, 451, 453, 456, 457, 459-464, 467-470, 494, 598 PP2 (protein phosphatase 2) 386, 451 PP2A (protein phosphatase 2A) 386, 451, 453, 459, 461, 464, 466-468, 598 PP2B 448, 451, 453-457, 459-462, 464, 469-471 Prefrontal cortex (PFC) 49, 59, 82, 114, 118, 119, 126, 127, 136, 143, 144, 146-152, 160-162, 171, 230, 239, 267, 314, 326, 340 Propranolol 83, 156, 160-162, 165, 167-169, 273 Protein kinase A see PKA Protein kinase C see PKC Protein synthesis 13, 98, 266, 268, 317, 321, 322, 331, 332, 362, 364, 369, 370, 373, 375, 379, 419, 427, 442, 448, 456, 459, 463, 492, 495-497, 500, 507, 508, 514-523, 529-539, 564, 568, 569, 574, 578 Protein synthesis inhibitor (PSI) 266, 268, 321, 322, 379, 492, 514, 515, 517-519, 521-523, 530, 531, 533, 569 Purine 196-198, 203, 205, 207, 210, 214, 516 R Reaction time 101, 113, 117, 118, 150, 241 Receptor-operated Ca2+ channel (ROCCs) 2, Reconsolidation 500, 521-523, 533-535 Reference memory (RM) 49-51, 98, 116, 128, 133, 134, 226, 228, 229, 231, 238, 259, 471, 485, 581-583 Index Reinforcement 51, 54, 120, 146, 163, 169, 174, 176, 178-180, 182, 185-187, 189, 251, 259, 268, 465, 466, 468, 470, 471 Retention 8, 27, 49, 51, 53, 72-85, 91, 99, 101, 116, 117, 132, 133, 135, 136, 144, 161-164, 167, 181-183, 186, 197, 240, 241, 246, 251, 256, 258-260, 262, 264-275, 277, 278, 295, 317-322, 340, 356-359, 375, 378, 391-394, 397, 398, 413, 414, 427, 437, 440, 464-470, 485-487, 516, 517, 520, 536, 537, 546, 554, 556, 573, 583, 597 Retinoic acid (RA) 586-588 Retrieval 31, 55, 61, 99, 103, 133, 136, 150, 162, 181, 186, 226, 228-237, 246, 256-258, 260-262, 267-269, 273, 275, 276, 279, 318, 324, 339, 340, 369, 372, 375, 378, 379, 391, 414, 416, 419, 432, 468, 485, 498, 500, 521, 533-535, 583 Reward 75, 78, 80, 118-121, 143, 145, 146, 151, 174, 176, 178, 180, 182, 186, 187, 189, 238, 241, 269, 393, 484, 582, 584, 586 Ryanodine receptor (RyR) 3, 5-8, 10, 11, 13, 14, 592 S Schizophrenia 144, 400 Scopolamine 90, 91, 99, 103, 132, 135, 136, 149, 150, 197, 198, 201, 207, 234, 240, 252, 254, 260, 268, 271-274, 288, 391, 570 Second messenger 39, 43, 61, 96, 125, 129, 144, 156, 157, 158, 259, 287, 349, 350, 351, 352, 356, 370, 375, 399, 426, 456, 493, 495, 534, 566, 591, 600 Sedation 90, 197 Self-administration 118, 119, 178 Self-stimulation 118, 146, 178-180, 189 Senescence 181, 583, 584, 586, 587 Serotonin 25, 26, 31, 33, 125-128, 130, 178, 225, 228, 261, 265, 269, 326, 351, 374, 400, 463, 495, 496, 519, 574, 598 Shaker 8, 20, 21, 25, 26, 27, 28, 32 Short-term facilitation 22, 26, 495 Short-term memory 28, 49, 99-101, 136, 166, 169, 226, 238-242, 254, 256, 264, 270, 339, 362, 364, 369, 370, 375, 376, 397, 429, 452, 470, 471, 492, 514, 531, 535, 576, 595 613 Signal detection 113, 241 Signal integration 20, 442, 455 Silent synapse 415, 417, 543, 556, 557 Sleep 91, 104, 155, 187, 234, 235, 266 Slow afterhyperpolarisation (sAHP) 8, 20, 22, 25, 29, 30, 33, 595 Somatostatin 263, 265, 266, 274, 277, 341 Spike patterning 20 Spine 413, 543, 546, 548-550, 553-559, 564566, 572, 573, 575, 577-579 Spontaneous alternation 50, 197, 198, 201, 207, 238, 268, 271, 272, 304, 485 State-dependency 76, 77 Storage 1, 4, 14, 72, 77, 79, 80, 83, 84, 91, 99, 103, 155, 161, 164, 186, 226, 271, 295, 314, 317, 320-322, 364, 370, 373, 401, 402, 411, 412, 427, 430, 440, 448, 449, 456, 458, 460-462, 471, 495, 498, 507, 511, 522, 531, 534, 535, 543, 545, 548, 559, 564, 567, 568, 574, 579, 582, 583, 586, 595 Store-operated Ca2+ channels (SOCCs) 2, Stress 4, 6, 12, 127, 132, 147, 151, 152, 162, 169, 182, 224, 261-265, 269, 271, 274, 302, 314-317, 320, 322, 324-326, 340, 390, 394, 395, 402, 403, 443, 506, 508, 511, 516, 531, 532 Striatum 50, 72, 81, 82, 93, 95, 130, 134, 143, 145, 149, 158, 159, 161, 178, 196, 197, 207, 210, 212, 270, 288, 296, 356, 391, 520, 578 Structural synaptic remodeling 543, 553 Substance P 270-272, 274, 277, 279 Substantia nigra 79, 81, 114, 130, 144, 176, 189, 225, 271, 276 Synaptic plasticity 1, 7, 9, 10, 12, 14, 20, 22, 25, 31, 43, 61, 98, 119, 187, 196, 198-200, 207, 210-212, 263, 276, 279, 286, 295, 300, 301, 304, 306, 309, 310, 320, 322, 323, 330, 335, 337, 343, 349, 351, 353-356, 358, 362, 383, 386-389, 401, 402, 411, 412, 417, 419, 425-429, 431, 433, 435, 439-441, 448, 455, 458, 461, 462, 470, 471, 480, 482, 487, 522, 523, 529, 550, 554, 567, 569, 570, 572-577, 579, 583, 586, 591, 600 Synaptogenesis 128, 514, 543, 544, 546-548, 553, 554, 558, 559, 573-575 614 From Messengers to Molecules: Memories Are Made of These T V Tachykinin 271, 272 Theta rhythm 98, 102, 133, 136, 137, 295, 435, 481 Trace eyeblink conditioning 29, 30, 96, 544, 547, 548, 550, 553, 554, 556, 557, 566, 592, 594-597 Transcription 3, 4, 5, 9, 10, 13, 14, 98, 259, 287, 315, 317, 330, 331, 336, 338, 340, 369, 370, 373, 375, 379, 415, 417, 418, 427, 449, 453, 456, 458, 492, 493, 495, 496, 498, 501, 507, 508, 511, 514, 516, 519, 520, 522, 523, 529-535, 539, 564, 574, 577, 591, 600 Transcription factor 10, 13, 98, 287, 315, 317, 331, 369, 370, 373, 415, 417, 418, 427, 429, 492, 493, 507, 508, 511, 514, 519, 522, 523, 529, 532-535, 539, 600 Transgenic mice 31, 133, 277, 361, 387, 390, 398, 401, 402, 419, 498, 500 Translation 449, 456, 496, 514, 516-518, 520, 522, 523, 531, 564, 567 TrkA 287-289, 295, 296 TrkB 287, 289 TrkC 287, 289 Trophic factor 196 Tuberomammillary nucleus (TM) 174-180, 182-185, 187-189, 384 Two peaks 369, 370, 375 Type phosphatase 451 Tyrosine kinase 98, 286, 287, 300-302, 304, 309, 310, 369, 426, 432, 494, 576 Vasopressin 256-260, 263, 265, 272-274, 277, 278, 314, 414 Voltage-gated Ca2+ channel 95, 98, 335, 352, 493, 592, 600 Voltage-operated Ca2+ channel 2, 336 Voltage-sensitive Ca2+ channel 337, 430 W Working memory (WM) 43, 44, 49-51, 95, 100-102, 113, 115-117, 120, 121, 132-134, 136, 143, 147-152, 161, 162, 197, 198, 201, 226, 228, 229, 231, 238, 259, 277, 340, 363, 397, 470, 471, 485, 581, 582 NEUROSCIENCE INTELLIGENCE UNIT N INTELLIGENCE UNITS Biotechnology Intelligence Unit Medical Intelligence Unit Molecular Biology Intelligence Unit Neuroscience Intelligence Unit Tissue Engineering Intelligence Unit 790306 478627 NIU From Messengers to Molecules: Memories Are Made of These The chapters in this book, as well as the chapters of all of the five Intelligence Unit series, are available at our website G RIEDEL • PLATT Landes Bioscience, a bioscience publisher, is making a transition to the internet as Eurekah.com F M ... INTELLIGENCE UNIT From Messengers to Molecules: Memories Are Made of These Gernot Riedel, Ph.D Bettina Platt, Ph.D School of Medical Sciences College of Life Sciences and Medicine University of Aberdeen... urged to carefully review and evaluate the information provided herein Library of Congress Cataloging-in-Publication Data From messengers to molecules : memories are made of these / [edited by]... Chapter 2.9 Oliver Stork Institute of Physiology University of Magdeburg Magdeburg, Germany Chapter 5.3 Edwin J Weeber Division of Neuroscience Baylor College of Medicine Houston, Texas, U.S.A