The Biology of Memory: A Forty-Year Perspective

In the forty years since the Society for Neuroscience was founded, our understanding of the biology of memory has progressed dramatically. From a historical perspective, one can discern four distinct periods of growth in neurobiological research during that time. Here I use that chronology to chart a personalized and selective course through forty years of extraordinary advances in our understanding of the biology of memory storage.

[1]  S. Tonegawa,et al.  The Essential Role of Hippocampal CA1 NMDA Receptor–Dependent Synaptic Plasticity in Spatial Memory , 1996, Cell.

[2]  Alcino J. Silva,et al.  Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein , 1994, Cell.

[3]  R. Nicoll,et al.  Auxiliary Subunits Assist AMPA-Type Glutamate Receptors , 2006, Science.

[4]  A. Routtenberg Chapter 18 Synaptic plasticity and protein kinase C , 1986 .

[5]  E. Kandel,et al.  Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. , 1993, Science.

[6]  Eric R. Kandel,et al.  A Neuronal Isoform of CPEB Regulates Local Protein Synthesis and Stabilizes Synapse-Specific Long-Term Facilitation in Aplysia , 2003, Cell.

[7]  E. Kandel,et al.  4.02 – Molecular Studies of Learning and Memory in Aplysia and the Hippocampus: A Comparative Analysis of Implicit and Explicit Memory Storage , 2008 .

[8]  E. Kandel,et al.  Cellular neurophysiological approaches in the study of learning. , 1968, Physiological reviews.

[9]  Eric R. Kandel,et al.  Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation , 1990, Nature.

[10]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[11]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[12]  R. Menzel,et al.  Learning and Memory in Bees , 1978 .

[13]  E R Kandel,et al.  Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Barry J Dickson,et al.  Function of the Drosophila CPEB protein Orb2 in long-term courtship memory , 2007, Nature Neuroscience.

[15]  E. Kandel,et al.  A Neuronal Isoform of the Aplysia CPEB Has Prion-Like Properties , 2003, Cell.

[16]  K. Deisseroth,et al.  Circuit-breakers: optical technologies for probing neural signals and systems , 2007, Nature Reviews Neuroscience.

[17]  A. Routtenberg Synaptic plasticity and protein kinase C. , 1986, Progress in brain research.

[18]  Barbara O Rothbaum,et al.  Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. , 2004, Archives of general psychiatry.

[19]  Eric R. Kandel,et al.  Long-Term Habituation of a Defensive Withdrawal Reflex in Aplysia , 1972, Science.

[20]  L. Nowak,et al.  Magnesium gates glutamate-activated channels in mouse central neurones , 1984, Nature.

[21]  Mark Mayford,et al.  Localization of a Stable Neural Correlate of Associative Memory , 2007, Science.

[22]  M. Wilson,et al.  Dentate Gyrus NMDA Receptors Mediate Rapid Pattern Separation in the Hippocampal Network , 2007, Science.

[23]  R S Zucker,et al.  Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. , 1988, Science.

[24]  K. Svoboda,et al.  Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. , 1999, Science.

[25]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[26]  R. Nicoll,et al.  An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation , 1989, Nature.

[27]  Joseph E LeDoux Emotion: clues from the brain. , 1995, Annual review of psychology.

[28]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[29]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[30]  Alcino J. Silva,et al.  Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. , 1992, Science.

[31]  James H. Schwartz,et al.  Ubiquitin C-Terminal Hydrolase Is an Immediate-Early Gene Essential for Long-Term Facilitation in Aplysia , 1997, Cell.

[32]  E. Kandel,et al.  Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. , 1976, Science.

[33]  R. Nicoll,et al.  Dynamin-dependent endocytosis of ionotropic glutamate receptors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. Dudchenko The hippocampus as a cognitive map , 2010 .

[35]  R. J. McDonald,et al.  A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. , 1993, Behavioral neuroscience.

[36]  E. Kandel,et al.  A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. Kandel,et al.  C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia , 1994, Cell.

[38]  S. Siegelbaum,et al.  Postsynaptic induction and presynaptic expression of hippocampal long-term depression. , 1994, Science.

[39]  E R Kandel,et al.  Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. , 1976, Science.

[40]  W. Quinn,et al.  Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila , 1994, Cell.

[41]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Craig W. Berridge,et al.  Stress-induced activation of prefrontal cortex dopamine turnover: blockade by lesions of the amygdala , 1994, Brain Research.

[43]  E R Kandel,et al.  Neuronal Mechanisms of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia , 1970, Science.

[44]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[45]  E. Kandel,et al.  Synapse-Specific, Long-Term Facilitation of Aplysia Sensory to Motor Synapses: A Function for Local Protein Synthesis in Memory Storage , 1997, Cell.

[46]  E. Kandel,et al.  Intracellular injection of t he catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Daniel L. Schacter,et al.  What are the memory systems of 1994 , 1994 .

[48]  Mary Chen,et al.  Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change , 1995, Cell.

[49]  Bruno Bontempi,et al.  Selective Erasure of a Fear Memory , 2009, Science.

[50]  R. Tsien,et al.  Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. , 1989, Science.

[51]  Roberto Malinow,et al.  Persistent protein kinase activity underlying long-term potentiation , 1988, Nature.

[52]  E. Kandel,et al.  Genetic and Pharmacological Evidence for a Novel, Intermediate Phase of Long-Term Potentiation Suppressed by Calcineurin , 1998, Cell.

[53]  T. Bliss,et al.  Optical Quantal Analysis Reveals a Presynaptic Component of LTP at Hippocampal Schaffer-Associational Synapses , 2003, Neuron.

[54]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[55]  S. R. Y. Cajal The Croonian lecture.—La fine structure des centres nerveux , 1894 .

[56]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[57]  M. Nicolelis,et al.  Remote Control of Neuronal Activity in Transgenic Mice Expressing Evolved G Protein-Coupled Receptors , 2009, Neuron.

[58]  T. Bliss,et al.  Optical Quantal Analysis Indicates That Long-Term Potentiation at Single Hippocampal Mossy Fiber Synapses Is Expressed through Increased Release Probability, Recruitment of New Release Sites, and Activation of Silent Synapses , 2004, The Journal of Neuroscience.

[59]  L. Abbott,et al.  Cascade Models of Synaptically Stored Memories , 2005, Neuron.

[60]  Ronald L. Davis,et al.  Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster , 1981, Nature.

[61]  W. Harris,et al.  Conditioned behavior in Drosophila melanogaster. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[62]  F. Krasne,et al.  Excitation and habituation of the crayfish escape reflex: the depolarizing response in lateral giant fibres of the isolated abdomen. , 1969, The Journal of experimental biology.

[63]  E. Kandel,et al.  Long-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors , 1991, Nature.

[64]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  E. Kandel,et al.  A genetic test of the effects of mutations in PKA on mossy fiber ltp and its relation to spatial and contextual learning , 1995, Cell.

[66]  K. Svoboda,et al.  Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice , 2008, Nature.

[67]  Eric R. Kandel,et al.  Long-Term Sensitization of a Defensive Withdrawal Reflex in Aplysia , 1973, Science.

[68]  E R Kandel,et al.  Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. , 1992, Science.

[69]  Karl Deisseroth,et al.  Improved expression of halorhodopsin for light-induced silencing of neuronal activity , 2008, Brain cell biology.

[70]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[71]  M. Fyhn,et al.  Spatial Representation in the Entorhinal Cortex , 2004, Science.

[72]  E R Kandel,et al.  Cellular analysis of long-term habituation of the gill-withdrawal reflex of Aplysia californica. , 1978, Science.

[73]  Eric R. Kandel,et al.  Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[74]  C. H. Bailey,et al.  Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Joel D. Richter,et al.  Cytoplasmic Polyadenylation in Development and Beyond , 1999, Microbiology and Molecular Biology Reviews.

[76]  M. Mayer,et al.  Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones , 1984, Nature.

[77]  David J. Anderson,et al.  Subregion- and Cell Type–Restricted Gene Knockout in Mouse Brain , 1996, Cell.

[78]  Benjamin R. Arenkiel,et al.  In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2 , 2007, Neuron.

[79]  E. Boyden,et al.  Selective Engagement of Plasticity Mechanisms for Motor Memory Storage , 2006, Neuron.

[80]  E. Kandel,et al.  Memory suppressor genes: inhibitory constraints on the storage of long-term memory. , 1998, Science.

[81]  E. Kandel,et al.  Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. , 1992, Science.

[82]  E. Kandel,et al.  Genetic Demonstration of a Role for PKA in the Late Phase of LTP and in Hippocampus-Based Long-Term Memory , 1997, Cell.

[83]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[84]  André A Fenton,et al.  PKMζ Maintains Spatial, Instrumental, and Classically Conditioned Long-Term Memories , 2008, PLoS biology.

[85]  H. Lorković Cellular Basis of Behavior: An Introduction to Behavioral Neurology , 1977 .

[86]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[87]  R. F. Thompson,et al.  Decrement of ventral root electrotonus and intracellularly recorded PSPs produced by iterated cutaneous afferent volleys. , 1966, Journal of neurophysiology.

[88]  E R Kandel,et al.  Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. , 1993, Science.

[89]  D. Kennedy,et al.  Neuronal Circuit Mediating Escape Responses in Crayfish , 1971, Science.

[90]  R. Rescorla,et al.  A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement , 1972 .

[91]  John F. Guzowski,et al.  Neuronal Competition and Selection During Memory Formation , 2006, Science.

[92]  Alcino J. Silva,et al.  Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. , 1992, Science.

[93]  E. Kandel,et al.  Control of Memory Formation Through Regulated Expression of a CaMKII Transgene , 1996, Science.

[94]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[95]  D. Alkon Associative Training of Hermissenda , 1974, The Journal of general physiology.

[96]  S. Ramón y Cajal,et al.  The Croonian lecture.—La fine structure des centres nerveux , 1894, Proceedings of the Royal Society of London.

[97]  R. Nicoll,et al.  A persistent postsynaptic modification mediates long-term potentiation in the hippocampus , 1988, Neuron.

[98]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[99]  A. Fine,et al.  Postsynaptic Calcium Transients Evoked by Activation of Individual Hippocampal Mossy Fiber Synapses , 2001, The Journal of Neuroscience.

[100]  Raag D. Airan,et al.  Temporally precise in vivo control of intracellular signalling , 2009, Nature.

[101]  T. Carew,et al.  Invertebrate learning and memory: from behavior to molecules. , 1986, Annual review of neuroscience.

[102]  Michael A Sutton,et al.  Parallel Molecular Pathways Mediate Expression of Distinct Forms of Intermediate-Term Facilitation at Tail Sensory–Motor Synapses in Aplysia , 2000, Neuron.

[103]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[104]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[105]  D. Jane,et al.  The glutamate story , 2006, British journal of pharmacology.