Hippocampal long-term depression: master or minion in declarative memory processes?

The neural mechanisms for the formation of declarative memory (memory for facts and events) are believed to be integrated from processes mediated by hippocampal long-term potentiation (LTP) and long-term depression (LTD). Traditionally, LTP has been designated as the main mediator of spatial memory storage in the hippocampus, whereas LTD has been assigned an auxiliary role in signal-to-noise regulation or in forgetting. It has recently become apparent, however, that LTD contributes directly to hippocampal information storage. In fact, LTD could dominate in the processing of precise spatial characteristics. Accumulating evidence supports the idea that LTP and LTD enable distinct and separate forms of information storage, which together facilitate the generation of a spatial cognitive map.

[1]  S Laroche,et al.  Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. , 1997, Journal of neurophysiology.

[2]  P. Dayan,et al.  Optimising synaptic learning rules in linear associative memories , 1991, Biological Cybernetics.

[3]  Trevor Sharp,et al.  A review of central 5-HT receptors and their function , 1999, Neuropharmacology.

[4]  Michael R. Hunsaker,et al.  The role of hippocampal subregions in detecting spatial novelty. , 2005, Behavioral neuroscience.

[5]  Paul E. Gilbert,et al.  A Behavioral Assessment of Hippocampal Function Based on a Subregional Analysis , 2004, Reviews in the neurosciences.

[6]  Tadaharu Tsumoto,et al.  Long-term depression in cerebral cortex: a possible substrate of “forgetting” that should not be forgotten , 1993, Neuroscience Research.

[7]  D. Manahan‐Vaughan,et al.  The 5-hydroxytryptamine4 receptor exhibits frequency-dependent properties in synaptic plasticity and behavioural metaplasticity in the hippocampal CA1 region in vivo. , 2005, Cerebral cortex.

[8]  J. Lisman,et al.  Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine , 2001, Hippocampus.

[9]  Thomas M. Sanderson,et al.  Tyrosine Phosphatases Regulate AMPA Receptor Trafficking during Metabotropic Glutamate Receptor-Mediated Long-Term Depression , 2006, The Journal of Neuroscience.

[10]  J. Wess,et al.  Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice , 2003, Molecular Psychiatry.

[11]  J. Krueger,et al.  Differences in spatial learning comparing transgenic p75 knockout, New Zealand Black, C57BL/6, and Swiss Webster mice , 2004, Behavioural Brain Research.

[12]  K. Mikoshiba,et al.  Impairment of hippocampal long‐term depression and defective spatial learning and memory in p35–/– mice , 2005, Journal of neurochemistry.

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

[14]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[15]  E. Wood,et al.  Dissociating the past from the present in the activity of place cells , 2006, Hippocampus.

[16]  Paul E. Gilbert,et al.  Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1 , 2001, Hippocampus.

[17]  Alex Martin,et al.  Access the most recent version at doi: 10.1101/lm.251906 , 2006 .

[18]  Lucia F Jacobs,et al.  Unpacking the cognitive map: the parallel map theory of hippocampal function. , 2003, Psychological review.

[19]  M. Sheng,et al.  Role of NMDA Receptor Subtypes in Governing the Direction of Hippocampal Synaptic Plasticity , 2004, Science.

[20]  Denise Manahan-Vaughan,et al.  Group 1 and 2 Metabotropic Glutamate Receptors Play Differential Roles in Hippocampal Long-Term Depression and Long-Term Potentiation in Freely Moving Rats , 1997, The Journal of Neuroscience.

[21]  M. Bear,et al.  Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. , 2000, Science.

[22]  D. Manahan‐Vaughan,et al.  Depotentiation in the dentate gyrus of freely moving rats is modulated by D1/D5 dopamine receptors. , 2000, Cerebral cortex.

[23]  R. Morris,et al.  Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas , 2006, The European journal of neuroscience.

[24]  E. Rolls,et al.  A computational theory of hippocampal function, and empirical tests of the theory , 2006, Progress in Neurobiology.

[25]  Thomas Straube,et al.  Requirement of β‐adrenergic receptor activation and protein synthesis for LTP‐reinforcement by novelty in rat dentate gyrus , 2003 .

[26]  Yasushi Miyashita,et al.  Cognitive Memory: Cellular and Network Machineries and Their Top-Down Control , 2004, Science.

[27]  D. Manahan‐Vaughan,et al.  Requirement of Translation But Not Transcription for the Maintenance of Long-Term Depression in the CA1 Region of Freely Moving Rats , 2000, The Journal of Neuroscience.

[28]  B. Derrick,et al.  NMDA receptor antagonists sustain LTP and spatial memory: active processes mediate LTP decay , 2002, Nature Neuroscience.

[29]  F. L. Jones,et al.  5-HT1a receptor antagonists block perforant path-dentate LTP induced in novel, but not familiar, environments. , 2006, Learning & memory.

[30]  W. Abraham,et al.  Induction and activity-dependent reversal of persistent LTP and LTD in lateral perforant path synapses in vivo , 2006, Neurobiology of Learning and Memory.

[31]  E. Moser,et al.  Spatial representation and the architecture of the entorhinal cortex , 2006, Trends in Neurosciences.

[32]  W. K. Cullen,et al.  Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty , 2003, Nature Neuroscience.

[33]  F. H. Lopes da Silva,et al.  Cortico‐hippocampal communication by way of parallel parahippocampal‐subicular pathways , 2000, Hippocampus.

[34]  B. Berger,et al.  Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat , 1985, Neuroscience.

[35]  P. Stanton,et al.  LTD, LTP, and the sliding threshold for long‐term synaptic plasticity , 1996, Hippocampus.

[36]  E. Rolls,et al.  A unified model of spatial and episodic memory , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  D. O. Hebb,et al.  The First Stage of Perception: Growth of the Assembly , 2005 .

[38]  J. Knierim,et al.  Hippocampal place cells: Parallel input streams, subregional processing, and implications for episodic memory , 2006, Hippocampus.

[39]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[40]  J. Frey,et al.  Reinforcement of rat hippocampal LTP by holeboard training. , 2005, Learning & memory.

[41]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[42]  J. Wess,et al.  M2 Muscarinic Acetylcholine Receptor Knock-Out Mice Show Deficits in Behavioral Flexibility, Working Memory, and Hippocampal Plasticity , 2004, The Journal of Neuroscience.

[43]  Wickliffe Abraham Stress‐related phenomena , 2004, Hippocampus.

[44]  I Izquierdo,et al.  Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. , 2000, Learning & memory.

[45]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[46]  J. Lisman,et al.  Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information , 2001, Hippocampus.

[47]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Bear,et al.  Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity , 2000, Nature.

[49]  Bai Lu,et al.  Activation of p75NTR by proBDNF facilitates hippocampal long-term depression , 2005, Nature Neuroscience.

[50]  Denise Manahan-Vaughan,et al.  Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  K. Hsu,et al.  Progress in Understanding the Factors Regulating Reversibility of Long-term Potentiation , 2001, Reviews in the neurosciences.

[52]  Mark F Bear,et al.  The mGluR theory of fragile X mental retardation , 2004, Trends in Neurosciences.

[53]  Michael J. Rowan,et al.  Behavioural stress facilitates the induction of long-term depression in the hippocampus , 1997, Nature.

[54]  E. Rolls,et al.  Neural networks and brain function , 1998 .

[55]  S. Becker A computational principle for hippocampal learning and neurogenesis , 2005, Hippocampus.

[56]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[57]  P. Dutar,et al.  Partial inhibition of PP1 alters bidirectional synaptic plasticity in the hippocampus , 2006, The European journal of neuroscience.

[58]  J. Bockaert,et al.  5-HT4 Receptors , 2012 .

[59]  D. Manahan‐Vaughan,et al.  Novelty acquisition is associated with induction of hippocampal long-term depression. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[60]  P. Dutar,et al.  Spatial learning and synaptic hippocampal plasticity in type 2 somatostatin receptor knock-out mice , 2002, Neuroscience.

[61]  E A Maguire,et al.  Hippocampal involvement in human topographical memory: evidence from functional imaging. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[62]  D. Manahan‐Vaughan,et al.  Persistent (>24h) long-term depression in the dentate gyrus of freely moving rats is not dependent on activation of NMDA receptors, L-type voltage-gated calcium channels or protein synthesis , 2007, Neuropharmacology.

[63]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

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

[65]  G. Lynch,et al.  Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 , 1986, Nature.

[66]  F. L. Jones,et al.  Novel Environments Enhance the Induction and Maintenance of Long-Term Potentiation in the Dentate Gyrus , 2004, The Journal of Neuroscience.

[67]  S. Sara,et al.  Network reset: a simplified overarching theory of locus coeruleus noradrenaline function , 2005, Trends in Neurosciences.

[68]  E. Kandel,et al.  A Role in Learning for SRF: Deletion in the Adult Forebrain Disrupts LTD and the Formation of an Immediate Memory of a Novel Context , 2006, Neuron.

[69]  D. Manahan‐Vaughan,et al.  Modulation by serotonin 5-HT(4) receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. , 2002, Cerebral cortex.

[70]  J. Frey,et al.  Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus , 2003, Neuroscience Letters.

[71]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[72]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

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

[74]  U. Heinemann,et al.  FM1-43 Imaging Reveals cGMP-Dependent Long-Term Depression of Presynaptic Transmitter Release , 2001, The Journal of Neuroscience.

[75]  M. Bear,et al.  Long-term depression in hippocampus. , 1996, Annual review of neuroscience.

[76]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[77]  N. Lemon,et al.  Dopamine D1/D5 Receptors Gate the Acquisition of Novel Information through Hippocampal Long-Term Potentiation and Long-Term Depression , 2006, The Journal of Neuroscience.

[78]  K. Mikoshiba,et al.  Calcineurin Plays Different Roles in Group II Metabotropic Glutamate Receptor- and NMDA Receptor-Dependent Long-Term Depression , 2002, The Journal of Neuroscience.

[79]  James J. Knierim,et al.  Ensemble Dynamics of Hippocampal Regions CA3 and CA1 , 2004, Neuron.

[80]  R. Morris,et al.  Glutamate-receptor-mediated encoding and retrieval of paired-associate learning , 2003, Nature.

[81]  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.

[82]  W. Abraham,et al.  A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation , 1999, Neuroscience.

[83]  T. Bonhoeffer,et al.  The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  D. Manahan‐Vaughan,et al.  Long-Term Depression: A Cellular Basis for Learning? , 2001, Reviews in the neurosciences.

[85]  Richard G M Morris,et al.  Distinct Contributions of Hippocampal NMDA and AMPA Receptors to Encoding and Retrieval of One-Trial Place Memory , 2005, The Journal of Neuroscience.

[86]  Yu Zhang,et al.  Synaptic Transmission and Plasticity in the Absence of AMPA Glutamate Receptor GluR2 and GluR3 , 2003, Neuron.

[87]  M. Yamada,et al.  Hippocampal long‐term depression as an index of spatial working memory , 2002, The European journal of neuroscience.