Memory: Mechanisms Other than LTP

Dominique Debanne, INSERM U641, Marseille, France
Emilie Campanac, Université de la Méditerranée, Marseille, France

Published online: September 2009

DOI: 10.1002/9780470015902.a0021398

Synaptic plasticity is not the exclusive mode of memory storage, and persistent regulation of voltage-gated ionic channels also participates in information storage. Long-term changes in neuronal excitability have been reported in several brain areas following learning. Synaptic activation of glutamate receptors initiates long-lasting modification in neuronal excitability at the pre- or postsynaptic side. Intrinsic plasticity is mediated by changes in the expression level or biophysical properties of ion channels in the membrane and can affect many different neuronal operations such as dendritic integration and action potential generation and propagation. Similarly to synaptic plasticity, long-lasting intrinsic plasticity is bidirectional and expresses a certain level of input or cell specificity. Synaptic and intrinsic plasticities not only share common learning rules and induction pathways but also contribute in synergy with these synaptic changes to the formation of a coherent mnesic engram.

Key concepts:

Synaptic plasticity is not the exclusive mode of memory storage, and persistent regulation of voltage-gated ionic channels also participates in information storage following learning. Synaptic activation of glutamate receptors initiates long-lasting modification in neuronal excitability at the pre- or postsynaptic side. Intrinsic plasticity is mediated by changes in the expression level or biophysical properties of ion channels in the membrane and can affect many different neuronal operations such as dendritic integration and action potential generation and propagation. Synaptic and intrinsic plasticities not only share common learning rules and induction pathways but also contribute in synergy with these synaptic changes to the formation of a coherent mnesic engram.

Keywords: nonsynaptic plasticity; E–S potentiation; LTP; dendrites; synaptic integration

Figure 1. Facilitation of the input–output function through the regulation of postsynaptic receptors or voltage-gated channels. (a) Persistent potentiation of synaptic transmission is characterized by enhanced postsynaptic current (EPSC). At the initial segment, the excitatory postsynaptic potential (EPSP) is large enough to cross the action potential (AP) threshold and to elicit a postsynaptic spike. (b) The same result is obtained if the AP threshold is hyperpolarized through the regulation of voltage-gated channels located at the cell body and/or axon initial segment. Note that here the synaptic current remains unchanged. (c) Enhanced amplification of the EPSP by voltage-gated channels located in the dendrite allows the generation of a postsynaptic AP without change in the EPSC.
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 References
    Abraham W, Gustafsson B and Wigström H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. Journal of Physiology 394: 367–380.
    Aizenman CD and Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nature Neuroscience 3: 109–111.
    Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226: 1037–1045.
    Alle H and Geiger JRP (2006) Combined analog and action potential coding in hippocampal mossy fibers. Science 311: 1290–1293.
    Andersen P, Sundberg SH, Sveen O, Swann JW and Wigström H (1980) Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea-pigs. Journal of Physiology 302: 463–482.
    Aou S, Woody CD and Birt D (1992) Increases in excitability of neurons of the motor cortex of cats after rapid acquisition of eye blink conditioning. Journal of Neuroscience 12: 560–569.
    Armano S, Rossi P, Taglietti V and D'Angelo E (2000) Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. Journal of Neuroscience 20: 5208–5216.
    Asztely F and Gustafsson B (1994) Dissociation between long-term potentiation and associated changes in field EPSP waveform in the hippocampal CA1 region: an in vitro study in guinea-pig brain slices. Hippocampus 4: 148–156.
    Beraneck M, Hachemaoui M, Idoux E et al. (2003) Long-term plasticity of ipsilateral medial vestibular nucleus neurons after unilateral labyrinthectomy. Journal of Neurophysiology 90: 184–203.
    Bliss TVP and Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforent path. Journal of Physiology 232: 331–356.
    Brembs B, Lorenzetti FD, Reyes FD, Baxter DA and Byrne JH (2002) Operant reward learning in Aplysia: neuronal correlates and mechanisms. Science 296: 1706–1709.
    Burrell BD, Sahley CL and Muller KJ (2001) Non-associative learning and serotonin induce similar bi-directional changes in excitability of a neuron critical for learning in the medicinal leech. Journal of Neuroscience 21: 1401–1412.
    Campanac E, Daoudal G, Ankri N and Debanne D (2008) Downregulation of dendritic Ih in CA1 pyramidal neurons after LTP. Journal of Neuroscience 28: 8635–8643.
    Campanac E and Debanne D (2008) Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons. Journal of Physiology 586: 779–793.
    Cleary LJ, Lee WL and Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. Journal of Neuroscience 18: 5988–5998.
    Cohen AS, Coussens CM, Raymond CR and Abraham WC (1999) Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. Journal of Neurophysiology 82: 3139–3148.
    Coulter DA, LoTurco JJ, Kubota M et al. (1989) Classical conditioning reduces amplitude and duration of calcium-dependent after-hyperpolarization in rabbit hippocampal pyramidal cells. Journal of Neurophysiology 61: 971–981.
    Cowan TM and Siegel RW (1986) Drosophila mutations that alter ionic conduction disrupt acquisition and retention of a conditioned odor avoidance response. Journal of Neurogenetics 3: 187–201.
    Daoudal G, Hanada Y and Debanne D (2002) Bi-directional plasticity of EPSP-spike coupling in CA1 hippocampal pyramidal neurons. Proceedings of the National Academy of Sciences of the USA 99: 14512–14517.
    Debanne D (2004) Information processing in the axon. Nature Reviews. Neuroscience 5: 304–316.
    Disterhoft JF, Coulter DA and Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proceedings of the National Academy of Sciences of the USA 83: 2733–2737.
    Egorov AV, Hamam BN, Fransen E, Hasselmo ME and Alonso A (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420: 173–178.
    Fricker A, Magee J and Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nature Neuroscience 7: 126–135.
    Ganguly K, Kiss L and Poo MM (2000) Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking. Nature Neuroscience 3: 1018–1026.
    Griffith LC, Wang J, Zhong Y, Wu CF and Greenspan RJ (1994) Calcium/calmodulin-dependent protein kinase II and potassium channel subunit eag similarly affect plasticity in Drosophila. Proceedings of the National Academy of Sciences of the USA 91: 10044–10048.
    Ireland DR and Abraham WC (2002) Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. Journal of Neurophysiology 88: 107–116.
    Kim J, Jung SC, Clemens AM, Petralia RS and Hoffman DA (2007) Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54: 933–947.
    Lai HC and Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nature Reviews. Neuroscience 7: 548–562.
    Li CY, Lu JT, Wu P, Duan SM and Poo MM (2004) Bidirectional modification of presynaptic excitability accompanying spike timing-dependent synaptic plasticity. Neuron 41: 257–268.
    Mellor J, Nicoll RA and Schmitz D (2002) Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295: 143–147.
    Melyan Z, Wheal HV and Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34: 107–114.
    Misonou H, Mohapatra DP, Park EW et al. (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nature Neuroscience 7: 711–718.
    Moyer JR, Thompson LT and Disterhoft JF (1996) Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. Journal of Neuroscience 16: 5536–5546.
    Mozzachiodi R, Lorenzetti FD, Baxter DA and Byrne JH (2008) Changes in neuronal excitability serve as a mechanism of long-term memory for operant conditioning. Nature Neuroscience 11: 1146–1148.
    Nelson AR, Gittis AH and du Lac S (2005) Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular nucleus neurons. Neuron 46: 623–631.
    Nelson AR, Krispel CM, Sekimjak C and du Lac S (2003) Long-lasting increases in intrinsic excitability triggered by inhibition. Neuron 40: 609–620.
    Oh MM, Kuo AG, Wu WW, Sametsky EA and Disterhoft JF (2003) Watermaze learning enhances excitability of CA1 pyramidal neurons. Journal of Neurophysiology 90: 2171–2179.
    Quirk MC, Blum KI and Wilson MA (2001) Experience-dependent changes in extracellular spike amplitude may reflect regulation of dendritic action-potential back-propagation in rat hippocampal pyramidal cells. Journal of Neuroscience 21: 240–248.
    Saar D, Grossman Y and Barkai E (1998) Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. European Journal of Neuroscience 10: 1518–1523.
    Scholz KP and Byrne JH (1987) Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235: 685–687.
    Schreurs BG, Tomsic D, Gusev PA and Alkon DL (1997) Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. Journal of Neurophysiology 77: 86–92.
    Sourdet V, Russier M, Daoudal G, Ankri N and Debanne D (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by mGluR5. Journal of Neuroscience 23: 10238–10248.
    Turrigiano GG and Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience 5: 97–107.
    Walmsley B, Berntson A, Leao RN and Fyffe REW (2006) Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways. Journal of Physiology 572: 313–321.
    Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends in Neuroscience 24: 455–463.
    Wang Z, Xu NI, Wu CP, Duan S and Poo MM (2003) Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 37: 463–472.
    Wathey JC, Lytton WW, Jester JM and Sejnowski TJ (1992) Computer simulations of EPSP-spike (E-S) potentiation in hippocampal CA1 pyramidal cells. Journal of Neuroscience 12: 607–618.
    Zhao ML and Wu CF (1997) Alterations in frequency coding and activity dependence of excitability in cultured neurons of Drosophila memory mutants. Journal of Neuroscience 17: 2187–2199.
 Further Reading
    Daoudal G and Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learning and Memory 10: 456–465.
    Kim SJ and Linden DJ (2007) Ubiquitous plasticity and memory storage. Neuron 56: 582–592.
    Sjöström PJ, Rancz EA, Roth A and Häusser M (2008) Dendritic excitability and synaptic plasticity. Physiological Reviews 88: 769–840.
    Zhang W and Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nature Reviews Neuroscience 4: 885–900.

Related Sub-Topics:

Learning and Memory: Cellular and Molecular Mechanisms
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Article Title: Memory: Mechanisms Other than LTP
 
How to Cite close
Debanne, Dominique, and Campanac, Emilie(Sep 2009) Memory: Mechanisms Other than LTP. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021398]