Article thumbnail

Presynaptic Ionotropic Receptors Controlling and Modulating the Rules for Spike Timing-Dependent Plasticity

By Matthijs B. Verhoog and Huibert D. Mansvelder

Abstract

Throughout life, activity-dependent changes in neuronal connection strength enable the brain to refine neural circuits and learn based on experience. In line with predictions made by Hebb, synapse strength can be modified depending on the millisecond timing of action potential firing (STDP). The sign of synaptic plasticity depends on the spike order of presynaptic and postsynaptic neurons. Ionotropic neurotransmitter receptors, such as NMDA receptors and nicotinic acetylcholine receptors, are intimately involved in setting the rules for synaptic strengthening and weakening. In addition, timing rules for STDP within synapses are not fixed. They can be altered by activation of ionotropic receptors located at, or close to, synapses. Here, we will highlight studies that uncovered how network actions control and modulate timing rules for STDP by activating presynaptic ionotropic receptors. Furthermore, we will discuss how interaction between different types of ionotropic receptors may create “timing” windows during which particular timing rules lead to synaptic changes

Topics: Review Article
Publisher: Hindawi Publishing Corporation
OAI identifier: oai:pubmedcentral.nih.gov:3173883
Provided by: PubMed Central

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.

Suggested articles

Citations

  1. (2006). A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons,”
  2. (1991). a r t i n ,G .A .B u s t o s
  3. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons,”
  4. (2003). Acetylcholinedependent potentiation of temporal frequency representation in the barrel cortex does not depend on response magnitude during conditioning,” J o u r n a lo fP h y s i o l o g yP a r i s ,
  5. (2000). Activitydependent induction of tonic calcineurin activity mediates a rapid developmental downregulation
  6. (2010). and long-term plasticity are not modulated by astrocyte
  7. (2007). andH.D.Mansvelder,“Increasedthresholdforspike-timingdependentplasticityiscausedbyunreliablecalciumsignaling in mice lacking fragile
  8. (2007). Astrocytes potentiate transmitter release at single hippocampal synapses,”
  9. (2006). Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo,”
  10. (2010). Axonal α7 nicotinic ACh receptors modulate presynaptic NMDA receptor expression and structural plasticity of glutamatergic presynaptic boutons,”
  11. (2006). Brain nicotinic acetylcholine receptors: native subtypes and their relevance,”
  12. (2004). Ca2+ permeability of nicotinic acetylcholine receptors,”
  13. (2004). Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling,”
  14. (2004). Calcium dynamics of cortical astrocytic networks in vivo,”
  15. (2000). Calcium stores regulate the polarity and input specificity of synaptic modification,”
  16. (1992). Calcium waves in astrocytes-filling in the gaps,”
  17. (2001). Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy,”
  18. (1997). Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections,”
  19. (2004). D u g u i da n dT .G .S m a r t ,“ R e t r o g r a d ea c t i v a t i o n of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses,”
  20. (2009). Defining pre-synaptic nicotinic receptors regulated by beta amyloid in mouse cortex and hippocampus with receptor null mutants,”
  21. (2008). Dendritic NMDA receptors activate axonal calcium channels,”
  22. (2000). Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex,”
  23. (2010). Dendritic synapse location and neocortical spike-timing-dependent plasticity,”
  24. (2007). Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long-term depression,”
  25. (2007). Distributed network actions by nicotine increase the threshold for spiketiming-dependent plasticity in prefrontal cortex,”
  26. (1996). Diversity of nicotinic acetylcholine receptors in rat brain. V. α-bungarotoxin-sensitive nicotinic receptors in olfactory bulb neurons and presynaptic modulation of glutamate release,”
  27. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. II. The rundown and inward rectification of agonist-elicited whole-cell currents and identification of receptor subunits by in situ hybridization,”
  28. (2008). Endocannabinoids mediate neuron-astrocytecommunication,”Neuron,vol.57,no .6,pp .
  29. (2010). Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes,”
  30. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses,”
  31. (1992). Expression of NMDA channels on cerebellar Purkinje cells acutely dissociated from newborn rats,”
  32. (1994). Formation and inactivation of endogenous cannabinoid anandamide in central neurons,”
  33. (2007). Glutamate exocytosis from astrocytes controls synaptic strength,”
  34. (1993). Glutamateinduced increases in intracellular free
  35. (1991). Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals,”
  36. (2011). Habenula “Cholinergic” neurons corelease glutamate and acetylcholine and activate postsynapticneuronsviadistincttransmissionmodes,”Neuron,vol.
  37. (2007). High speed two-photon imaging of calciumdynamicsindendriticspines:consequencesforspine calcium kinetics and buffer capacity,”
  38. (2010). Human synapses show a wide temporal window for spiketiming-dependent plasticity,” Frontiers
  39. (2006). I.Duguida ndP .J .Sj¨ ostr¨ om,“Novel presynapticmechanisms for coincidence detection in synaptic plasticity,”
  40. (2002). Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar longterm depression,”
  41. (2000). J.L.FisherandJ.A.Dani,“Nicotinicreceptorsonhippocampal cultures can increase synaptic glutamate currents while decreasing the NMDA-receptor component,”
  42. (2006). L i e n ,Y .M u ,M .V a r g a s - C a b a l l e r o ,a n dM .M .P o o , “Visual stimuli-induced LTD of GABAergic synapses mediated by presynaptic NMDA receptors,”
  43. (2006). Learning induces long-term potentiation in the hippocampus,”
  44. (2006). Learning rules for spike timing-dependent plasticity depend on dendritic synapselocation,”TheJournalofNeuroscience,vol.26,no.41,
  45. (2010). Long-term potentiation depends on release of dserine from astrocytes,”
  46. (2000). Long-term potentiation of excitatory inputs to brain reward areas by nicotine,”
  47. (1998). Longterm synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures,”
  48. (2006). Malleability of spiketiming-dependent plasticity at the CA3-CA1 synapse,”
  49. (2005). Map plasticity in somatosensory cortex,”
  50. (2010). Mechanisms involved in systemic nicotine-induced glutamatergicsynapticplasticityondopamineneuronsinthe ventral tegmental area,”
  51. (2009). Mierau,Y.P.Auberson,andO.Paulsen,“Doubledissociation of spike timing-dependent potentiation and depression by subunit-preferring NMDA receptor antagonists in mouse barrelcortex,”CerebralCortex,vol.19,no.12,pp.2959–2969,
  52. (1996). N.BerrettaandR.S.G.Jones,“T onicfacilitationofglutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex,”
  53. (2011). Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses,”
  54. (2003). Neuroprotection by nicotine in mouse primary cortical cultures involves activation of calcineurin and L-type calcium channel inactivation,”
  55. (2009). Neuroscience: Glia—more than just brain glue,”
  56. (2007). Nicotine and synaptic plasticity in prefrontal cortex,”
  57. (1995). Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors,”
  58. (2003). Nicotinic acetylcholine receptors: from structure to brain function,”
  59. (1993). Nicotinic acid and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex
  60. (1995). Nicotinic receptor function in the mammalian central nervous system,”
  61. (1998). Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission,”TheJournalofNeuroscience,vol.18,no.18,pp. 7075–7083,
  62. (2002). Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes,”
  63. (1993). NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms,”
  64. (1994). o n y e r ,N .B u r n a s h e v ,D .J .L a u r i e ,B .S a k m a n n ,a n dP
  65. (2008). o r l e w ,D .J .B r a s i e r ,D .E .F e l d m a n ,a n dB .D .P h i l p o t , “Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity,”
  66. (2008). P.S.PinheiroandC.Mulle,“Presynapticglutamatereceptors: physiological functions and mechanisms of action,”
  67. (1998). Petrocellis, “Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action,”
  68. (2009). Phasic acetylcholine release and the volume transmission hypothesis: time to move on,”
  69. (2004). Precise localization of α7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area,”
  70. (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales,”
  71. (2008). Presynaptic and postsynaptic NMDA receptors mediate distinct effects of brain-derived neurotrophic factor on synaptic transmission,”
  72. (2004). Presynaptic ionotropic receptors and control of transmitter release,”
  73. (2008). Presynaptic ionotropic receptors,”
  74. (1972). Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses,”
  75. (1997). Presynaptic nicotinic ACh receptors,” Trends in Neurosciences,
  76. (2010). Presynaptic NMDA receptors and spike timing-dependent depression at cortical synapses,”
  77. (2009). Presynaptic NMDA receptors,”
  78. (1999). Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area,”
  79. (1996). r a y ,A .S .R a j a n ,K .A .R a d c l i
  80. receptors exert a permissive role on the activation of release-enhancing presynaptic α7 nicotinic receptors co-existing on rat neocortex glutamatergic terminals,”
  81. (2000). S.Laroche,S.Davis,andT.M.Jay,“Plasticityathippocampal to prefrontal cortex synapses: dual roles in working memory andconsolidation,”Hippocampus,vol.10,no.4,pp.438–446,
  82. (2009). Selective expression of ligandgated ion channels in L5 pyramidal cell axons,”
  83. (2002). Short-term synaptic plasticity,”
  84. (2003). Sj¨ ostr¨ o m ,G .G .T u r r i g i a n o ,a n dS .B .N e l s o n ,“ N e o c o r t i -cal LTD via coincident activation of presynaptic NMDA and cannabinoid receptors,”
  85. (2008). Spike timing-dependent plasticity: a hebbian learning rule,”
  86. (2008). Spike timingdependent long-term depression requires presynaptic NMDA receptors,”
  87. (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type,”
  88. (2005). Synaptic plasticity at hippocampal mossy fibre synapses,”
  89. (1997). Synaptic plasticity in a cerebellum-like structure depends on temporal order,”
  90. (1998). Synaptic potentials mediated via α-bungarotoxinsensitivenicotinicacetylcholinereceptorsinrathippocampal interneurons,”TheJournalofNeuroscience,vol.18,no.20,pp. 8228–8235,
  91. (2002). T s a y ,a n dR .Y u s t e ,“ C a l c i u md y n a m i c so f spines depend on their dendritic location,”
  92. (1983). Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus,”
  93. (1999). The glutamate receptor ion channels,”
  94. (1994). The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1,”
  95. (2006). The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation,”
  96. (1999). The α7 nicotinic acetylcholine receptor in neuronal plasticity,”
  97. (2001). Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity,”
  98. (2009). Tripartite synapses: astrocytes process and control synaptic information,”
  99. (1999). Tripartite synapses: glia, the unacknowledged partner,”
  100. (2006). Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex,”
  101. (1987). u s t a f s s o n ,H .W i g s t r o m ,W .C .A b r a h a m ,a n dY .Y . Huang, “Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to singlevolleysynapticpotentials,”TheJournalofNeuroscience,
  102. (1992). u s t o s ,J .A b a r c a ,M .I .F o r r a y ,K .G y s l i n g ,C .W .B r a d
  103. (1997). ubke,M.Frotscher,andB.Sakmann,“Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs,”
  104. (2001). Ultrastructural distribution of the α7 nicotinic acetylcholine receptor subunit in rat hippocampus,”
  105. (2004). V.Gundersen,J.L.Galbete etal.,“Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate,”
  106. (2003). Y.Humeau,H.Shaban,S.Bissi` ere,andA.L¨ uthi,“Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain,”
  107. (2000). α-Bungarotoxin-sensitive nicotinic receptors indirectly modulate [3H]dopamine release in rat striatalslices via glutamate release,”