Functional MRI of long-term potentiation: imaging network plasticity

Neurons are able to express long-lasting and activity-dependent modulations of their synapses. This plastic property supports memory and conveys an extraordinary adaptive value, because it allows an individual to learn from, and respond to, changes in the environment. Molecular and physiological changes at the cellular level as well as network interactions are required in order to encode a pattern of synaptic activity into a long-term memory. While the cellular mechanisms linking synaptic plasticity to memory have been intensively studied, those regulating network interactions have received less attention. Combining high-resolution fMRI and in vivo electrophysiology in rats, we have previously reported a functional remodelling of long-range hippocampal networks induced by long-term potentiation (LTP) of synaptic plasticity in the perforant pathway. Here, we present new results demonstrating an increased bilateral coupling in the hippocampus specifically supported by the mossy cell commissural/associational pathway in response to LTP. This fMRI-measured increase in bilateral connectivity is accompanied by potentiation of the corresponding polysynaptically evoked commissural potential in the contralateral dentate gyrus and depression of the inactive convergent commissural pathway to the ipsilateral dentate. We review these and previous findings in the broader context of memory consolidation.

[1]  C. Mathiesen,et al.  Modification of activity‐dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex , 1998, The Journal of physiology.

[2]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[3]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[4]  Jonathan R. Whitlock,et al.  Learning Induces Long-Term Potentiation in the Hippocampus , 2006, Science.

[5]  P Gloor,et al.  Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. , 1990, Brain : a journal of neurology.

[6]  E T Rolls,et al.  Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network , 1992, Hippocampus.

[7]  D. Amaral,et al.  The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus , 1985, Journal of neurocytology.

[8]  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.

[9]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[10]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[11]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

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

[13]  R G M Morris,et al.  Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[15]  N. Logothetis,et al.  Electric stimulation fMRI of the perforant pathway to the rat hippocampus. , 2008, Magnetic resonance imaging.

[16]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[17]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[18]  G. Lynch,et al.  A neurophysiological analysis of commissural projections to dentate gyrus of the rat. , 1975, Journal of neurophysiology.

[19]  Simon W. Moore,et al.  Efficient Physical Embedding of Topologically Complex Information Processing Networks in Brains and Computer Circuits , 2010, PLoS Comput. Biol..

[20]  C. Gilbert,et al.  Top-Down Reorganization of Activity in the Visual Pathway after Learning a Shape Identification Task , 2005, Neuron.

[21]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. W. Rudy,et al.  The hippocampal indexing theory and episodic memory: Updating the index , 2007, Hippocampus.

[23]  Oiwi Parker Jones,et al.  A Computational Approach , 2008 .

[24]  P. Andersen,et al.  Synaptic potentiation in the rat dentate gyrus during exploratory learning. , 1993, NeuroReport.

[25]  R. Morris,et al.  Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. , 2010, Annual review of psychology.

[26]  W. Blume,et al.  Auras, seizure focus, and psychiatric disorders. , 2000, Neuropsychiatry, neuropsychology, and behavioral neurology.

[27]  Masahiko Watanabe,et al.  Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors , 2008, Proceedings of the National Academy of Sciences.

[28]  G. A. Clark,et al.  Increased responsivity of dentate granule cells during nictitating membrane response conditioning in rabbit , 1984, Behavioural Brain Research.

[29]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[30]  Ryosuke Kawakami,et al.  Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. , 2003, Science.

[31]  N. Logothetis,et al.  Functional MRI Evidence for LTP-Induced Neural Network Reorganization , 2009, Current Biology.

[32]  D. Olton,et al.  Spatial memory and hippocampal function , 1979, Neuropsychologia.

[33]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[34]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[35]  F. Roman,et al.  Olfactory Associative Discrimination: A Model for Studying Modifications of Synaptic Efficacy in Neuronal Networks Supporting Long-term Memory , 2004, Reviews in the neurosciences.

[36]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[37]  Lucia M. Talamini,et al.  Recall of memory sequences by interaction of the dentate and CA3: A revised model of the phase precession , 2005, Neural Networks.

[38]  Jianrong Tang,et al.  Potentiated amygdaloid auditory-evoked potentials and freezing behavior after fear conditioning in mice , 2001, Brain Research.

[39]  A. Treisman The binding problem , 1996, Current Opinion in Neurobiology.

[40]  R. Morris,et al.  Impaired spatial learning after saturation of long-term potentiation. , 1998, Science.

[41]  B. Bontempi,et al.  Time-dependent reorganization of brain circuitry underlying long-term memory storage , 1999, Nature.

[42]  Patricia S. Goldman TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

[43]  Masahiko Watanabe,et al.  Target-Cell-Specific Left-Right Asymmetry of NMDA Receptor Content in Schaffer Collateral Synapses in ϵ1/NR2A Knock-Out Mice , 2004, The Journal of Neuroscience.

[44]  M. Yeckel,et al.  Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G. Golarai,et al.  Functional alterations in the dentate gyrus after induction of long-term potentiation, kindling, and mossy fiber sprouting. , 1996, Journal of neurophysiology.

[46]  M. Honda,et al.  Behavioral / Systems / Cognitive Functionally Segregated Neural Substrates for Arbitrary Audiovisual Paired-Association Learning , 2005 .

[47]  T. Bliss,et al.  Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide , 2013, Molecular Brain.

[48]  Yutaka Kirino,et al.  Time-Dependent Reorganization of the Brain Components Underlying Memory Retention in Trace Eyeblink Conditioning , 2003, The Journal of Neuroscience.

[49]  J. Sarvey,et al.  Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: Evidence for interhemispheric communication , 1996, The Journal of comparative neurology.

[50]  S. R. Cajal Textura del Sistema Nervioso del Hombre y de los Vertebrados, 1899–1904 , 2019 .

[51]  T. Lømo,et al.  Patterns of activation in a monosynaptic cortical pathway: The perforant path input to the dentate area of the hippocampal formation , 2004, Experimental Brain Research.

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

[53]  Santiago Canals,et al.  Neurophysiological, metabolic and cellular compartments that drive neurovascular coupling and neuroimaging signals , 2013, Front. Neuroenergetics.

[54]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[55]  S. Dehaene,et al.  Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework , 2001, Cognition.

[56]  James L. McClelland Parallel Distributed Processing , 2005 .

[57]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[58]  R. Gervais,et al.  Olfactory fear conditioning induces field potential potentiation in rat olfactory cortex and amygdala. , 2004, Learning & memory.

[59]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[60]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[61]  Yasushi Miyashita,et al.  Towards understanding of the cortical network underlying associative memory , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[62]  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.

[63]  C. Mathiesen,et al.  Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis , 2000, The Journal of physiology.

[64]  G. Golarai,et al.  Bilateral organization of parallel and serial pathways in the dentate gyrus demonstrated by current-source density analysis in the rat. , 1996, Journal of neurophysiology.

[65]  P Andersen,et al.  Entorhinal activation of dentate granule cells. , 1966, Acta physiologica Scandinavica.

[66]  Matthew A. Wilson,et al.  Hippocampal Memory Formation, Plasticity, and the Role of Sleep , 2002, Neurobiology of Learning and Memory.

[67]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[68]  Angelo Bifone,et al.  A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: Application to pharmacological MRI , 2006, NeuroImage.

[69]  T. Bliss,et al.  Lamellar organization of hippocampal excitatory pathways , 1971, Experimental Brain Research.

[70]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[71]  G Buzsáki,et al.  Hebbian modification of a hippocampal population pattern in the rat , 1999, The Journal of physiology.

[72]  Agnès Gruart,et al.  Involvement of the CA3–CA1 Synapse in the Acquisition of Associative Learning in Behaving Mice , 2006, The Journal of Neuroscience.

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

[74]  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.

[75]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[76]  B. McNaughton,et al.  Hippocampal synaptic enhancement and information storage within a distributed memory system , 1987, Trends in Neurosciences.

[77]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[78]  D. Marr A theory for cerebral neocortex , 1970, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[79]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[80]  Philipp Slusallek,et al.  Introduction to real-time ray tracing , 2005, SIGGRAPH Courses.

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

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

[83]  Karl Deisseroth,et al.  Hemisphere-specific optogenetic stimulation reveals left-right asymmetry of hippocampal plasticity , 2011, Nature Neuroscience.

[84]  Bibiana Scelfo,et al.  Long-Term Synaptic Changes Induced in the Cerebellar Cortex by Fear Conditioning , 2004, Neuron.

[85]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[86]  Edward Groth,et al.  Facts and hypotheses , 1999, Nature Biotechnology.

[87]  Aaron R. Seitz,et al.  Benefits of multisensory learning , 2008, Trends in Cognitive Sciences.

[88]  Joseph E LeDoux,et al.  Postsynaptic Receptor Trafficking Underlying a Form of Associative Learning , 2005, Science.

[89]  Nikolas Offenhauser,et al.  Principal neuron spiking: neither necessary nor sufficient for cerebral blood flow in rat cerebellum , 2004, The Journal of physiology.

[90]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[91]  H. Scharfman,et al.  Hilar mossy cells of the dentate gyrus: a historical perspective , 2013, Front. Neural Circuits.

[92]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[93]  D. Amaral A golgi study of cell types in the hilar region of the hippocampus in the rat , 1978, The Journal of comparative neurology.

[94]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[95]  D. Amaral,et al.  Hippocampal‐neocortical interaction: A hierarchy of associativity , 2000, Hippocampus.

[96]  E. J. Tehovnik,et al.  Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque , 2005, Neuron.

[97]  G. Teskey,et al.  Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation , 2004, Neuroscience.

[98]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[99]  Yu Ohmura,et al.  Regulation of cerebral blood flow in the hippocampus by neuronal activation through the perforant path: Relationship between hippocampal blood flow and neuronal plasticity , 2011, Brain Research.

[100]  Bruno Bontempi,et al.  Fast track to the medial prefrontal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[101]  S. Laurberg,et al.  Associational and commissural collaterals of neurons in the hippocampal formation (Hilus fasciae dentatae and subfield CA3) , 1981, Brain Research.

[102]  H. Scharfman,et al.  A role for hilar cells in pattern separation in the dentate gyrus: A computational approach , 2009, Hippocampus.

[103]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[104]  B. McNaughton,et al.  Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[105]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[106]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[107]  Natalie L. M. Cappaert,et al.  The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network , 2009, Nature Reviews Neuroscience.

[108]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[109]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

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