Bidirectional Hebbian Plasticity at Hippocampal Mossy Fiber Synapses on CA3 Interneurons

Galván, Emilio J.; Calixto, Eduardo; Barrionuevo, Germán

doi:10.1523/jneurosci.4848-08.2008

Cited by 59 publications

(112 citation statements)

References 99 publications

(161 reference statements)

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“…Ca 2þ mobilizes a retrograde signal in a PKA-dependent manner (Jaffe and Johnston 1990;Kapur et al 1998;Yeckel et al 1999). A similar mechanism has recently been reported at some MF to CA3 interneuron synapses (Galvan et al 2008(Galvan et al , 2010. This induction model is consistent with Hebbian MF-LTP (Urban and Barrionuevo 1996) whereby plasticity is triggered by both presynaptic activity that releases glutamate to activate postsynaptic group I mGluRs, and postsynaptic depolarization to activate L-type VGCCs.…”

Section: Mossy Fiber To Ca3 Pyramidal Cell Synapse As a Model For Presupporting

confidence: 79%

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Castillo

2011

Cold Spring Harbor Perspectives in Biology

145

134

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Ubiquitous forms of long-term potentiation (LTP) and depression (LTD) are caused by enduring increases or decreases in neurotransmitter release. Such forms or presynaptic plasticity are equally observed at excitatory and inhibitory synapses and the list of locations expressing presynaptic LTP and LTD continues to grow. In addition to the mechanistically distinct forms of postsynaptic plasticity, presynaptic plasticity offers a powerful means to modify neural circuits. A wide range of induction mechanisms has been identified, some of which occur entirely in the presynaptic terminal, whereas others require retrograde signaling from the postsynaptic to presynaptic terminals. In spite of this diversity of induction mechanisms, some common induction rules can be identified across synapses. Although the precise molecular mechanism underlying long-term changes in transmitter release in most cases remains unclear, increasing evidence indicates that presynaptic LTP and LTD can occur in vivo and likely mediate some forms of learning.A t several excitatory and inhibitory synapses, neuronal activity can trigger enduring increases or decreases in neurotransmitter release, thereby producing long-term potentiation (LTP) or long-term depression (LTD) of synaptic strength, respectively. In the last decade, many studies have revealed that these forms of plasticity are ubiquitously expressed in the mammalian brain, and accumulating evidence indicates that they may underlie behavioral adaptations occurring in vivo. These studies have also uncovered a wide range of induction mechanisms, which converge on the presynaptic terminal where an enduring modification in the neurotransmitter release process takes place. Interestingly, presynaptic forms of LTP/ LTD can coexist with classical forms of postsynaptic plasticity. Such diversity expands the dynamic range and repertoire by which neurons modify their synaptic connections. This review discusses mechanistic aspects of presynaptic LTP and LTD at both excitatory and inhibitory synapses in the mammalian brain, with an emphasis on recent findings. INDUCTION MECHANISMSAs illustrated in Figure 1, presynaptic LTP/LTD at both excitatory and inhibitory synapses can be induced in a homosynaptic or heterosynaptic manner, with induction occurring either entirely at the presynaptic terminal or requiring a retrograde messenger arising from the postsynaptic neuron. Each of these four induction

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Section: Mossy Fiber To Ca3 Pyramidal Cell Synapse As a Model For Presupporting

confidence: 79%

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Castillo

2011

Cold Spring Harbor Perspectives in Biology

145

134

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“…To investigate the mechanisms that contribute to the afferentspecific plasticity at PII inputs, we asked whether the presence or (Tó th and McBain, 1998;Tó th et al, 2000;Kullmann and Lamsa, 2007;Lamsa et al, 2007;Galván et al, 2008). …”

Section: Afferent-specific Expression Of Ca 2؉ -Permeable Ampar and Nmentioning

confidence: 99%

“…Basket cells express voltagedependent Ca 2ϩ channels (VDCCs) on their soma and proximal dendrites (Aponte et al, 2008;Bucurenciu et al, 2008). Ca 2ϩ entry through these channels during action potentials could support LTP induction at proximal MF inputs (Galván et al, 2008;Topolnik et al, 2009). Furthermore, group I mGluRs may contribute to Ca 2ϩ entry into interneurons, boosted by the strong postsynaptic depolarization such as during action potentials (Topolnik et al, 2005).…”

Section: Molecular Mechanisms Of Synapse-specific Plasticitymentioning

confidence: 99%

“…There are also differences in LTP induction: whereas in MF-PII synapses it depends on postsynaptic depolarization, MF-SLIN-mediated LTP emerges at resting potential. In stratum lacunosum-moleculare interneurons (SM), a Hebbian form of LTP was observed requiring strong depolarization during high-frequency stimulation (Galván et al, 2008). Similar to MF-PII and MF-SLIN synapses, LTP at MF-SM inputs is independent of NMDARs (Pelkey et al, 2005) and requires CI-AMPARs (Galván et al, 2008).…”

Section: Molecular Mechanisms Of Synapse-specific Plasticitymentioning

confidence: 99%

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Associative Plasticity at Excitatory Synapses Facilitates Recruitment of Fast-Spiking Interneurons in the Dentate Gyrus

Sambandan¹,

Sauer²,

Vida³

et al. 2010

J. Neurosci.

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Fast-spiking perisomatic-inhibitory interneurons (PIIs-permeable AMPARs and do not show plasticity on associative activation. Thus, precise recruitment of PIIs requires excitation through MF-PII synapses during feedforward activation. We propose that associative plasticity at these synapses is a central mechanism that adjusts inhibition levels to maintain sparse activity and to improve signal-to-noise ratio in the DG network.

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“…Even though it is believed that the laminar position of somata does not serve as a criterion for interneuron subtype classification in CA1 [43], position-dependent plasticity properties and anatomical characteristics of CA3 interneurons may enable a classification scheme for these cells based partially on somatic position [6,26,27]. Interestingly, stratum radiatum (R) and stratum lacunosum-moleculare (L-M) CA3 interneurons have similar morphological features in that their axons tend toward the hippocampal fissure [6]-impinging on R and L-M lamina of CA3-where recurrent collateral (RC) inputs terminate.…”

Section: Introductionmentioning

confidence: 99%

Properties and functional implications of I h in hippocampal area CA3 interneurons

Anderson

Galván

Mauna

et al. 2011

Pflugers Arch - Eur J Physiol

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The present study examines the biophysical properties and functional implications of I (h) in hippocampal area CA3 interneurons with somata in strata radiatum and lacunosum-moleculare. Characterization studies showed a small maximum h-conductance (2.6 ± 0.3 nS, n = 11), shallow voltage dependence with a hyperpolarized half-maximal activation (V (1/2) = -91 mV), and kinetics characterized by double-exponential functions. The functional consequences of I (h) were examined with regard to temporal summation and impedance measurements. For temporal summation experiments, 5-pulse mossy fiber input trains were activated. Blocking I (h) with 50 μM ZD7288 resulted in an increase in temporal summation, suggesting that I (h) supports sensitivity of response amplitude to relative input timing. Impedance was assessed by applying sinusoidal current commands. From impedance measurements, we found that I (h) did not confer theta-band resonance, but flattened the impedance-frequency relations instead. Double immunolabeling for hyperpolarization-activated cyclic nucleotide-gated proteins and glutamate decarboxylase 67 suggests that all four subunits are present in GABAergic interneurons from the strata considered for electrophysiological studies. Finally, a model of I (h) was employed in computational analyses to confirm and elaborate upon the contributions of I (h) to impedance and temporal summation.

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Bidirectional Hebbian Plasticity at Hippocampal Mossy Fiber Synapses on CA3 Interneurons

Cited by 59 publications

References 99 publications

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Associative Plasticity at Excitatory Synapses Facilitates Recruitment of Fast-Spiking Interneurons in the Dentate Gyrus

Properties and functional implications of I h in hippocampal area CA3 interneurons

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