Frequency Facilitation at Mossy Fiber-CA3 Synapses of Freely Behaving Rats Contributes to the Induction of Persistent LTD via an Adenosine-A1 Receptor-Regulated Mechanism

Hagena, Hardy; Manahan‐Vaughan, Denise

doi:10.1093/cercor/bhp184

Cited by 32 publications

(29 citation statements)

References 66 publications

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“…Thus, stimulation intensity during LFS was increased to evoke responses that reflect fEPSPs that comprise 70% of the maximum obtained in the input-output curve. LFS given at this intensity evokes persistent LTD in Sc-CA1 synapses (Manahan-Vaughan and Braunewell, 1999, 2005; Kemp and Manahan-Vaughan, 2004) and in mossy fiber- CA3 synapses(Hagena and Manahan-Vaughan, 2010). Interestingly, increasing the stimulation intensity during LFS resulted in synaptic potentiation (<3 h) at the pp-CA1 synapse in vivo .…”

Section: Discussionmentioning

confidence: 99%

“…In all hippocampal structures studied in our laboratory to date, low-frequency stimulation (LFS) consisting of 900 or 600 pulses at 1 Hz, has been shown to be effective in eliciting LTD and STD, respectively in Wistar rats (Manahan-Vaughan, 1997, 2000; Manahan-Vaughan and Braunewell, 1999; Kemp and Manahan-Vaughan, 2004; Poschel and Manahan-Vaughan, 2007; Hagena and Manahan-Vaughan, 2010). Therefore, this protocol was used to study synaptic depression at pp-CA1 synapses.…”

Section: Electrophysiological Recordingsmentioning

confidence: 99%

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The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing

Aksoy‐Aksel¹,

Manahan‐Vaughan²

2013

Front. Synaptic Neurosci.

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In terms of its sub-regional differentiation, the hippocampal CA1 region receives cortical information directly via the perforant (temporoammonic) path (pp-CA1 synapse) and indirectly via the tri-synaptic pathway where the last relay station is the Schaffer collateral-CA1 synapse (Sc-CA1 synapse). Research to date on pp-CA1 synapses has been conducted predominantly in vitro and never in awake animals, but these studies hint that information processing at this synapse might be distinct to processing at the Sc-CA1 synapse. Here, we characterized synaptic properties and synaptic plasticity at the pp-CA1 synapse of freely behaving adult rats. We observed that field excitatory postsynaptic potentials at the pp-CA1 synapse have longer onset latencies and a shorter time-to-peak compared to the Sc-CA1 synapse. LTP (>24 h) was successfully evoked by tetanic afferent stimulation of pp-CA1 synapses. Low frequency stimulation evoked synaptic depression at Sc-CA1 synapses, but did not elicit LTD at pp-CA1 synapses unless the Schaffer collateral afferents to the CA1 region had been severed. Paired-pulse responses also showed significant differences. Our data suggest that synaptic plasticity at the pp-CA1 synapse is distinct from the Sc-CA1 synapse and that this may reflect its specific role in hippocampal information processing.

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Section: Discussionmentioning

confidence: 99%

Section: Electrophysiological Recordingsmentioning

confidence: 99%

The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing

Aksoy‐Aksel¹,

Manahan‐Vaughan²

2013

Front. Synaptic Neurosci.

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“…To avoid an influence on fEPSPs mediated by DCG-IV on subsequent experiments, it was ensured that potentials had fully recovered before those experiments were performed. In addition, routine studies were conducted to verify that NMDAR-dependent LTP was not evident in these synapses, as described previously (Hagena and Manahan-Vaughan, 2010). Here, 30 min before tetanisation to induce LTP, the NMDAR antagonist, D-(-)-2-amino-5-phosphonopentanoic acid (D-AP5) was applied to examine whether LTP was influenced by the antagonist.…”

Section: Methodsmentioning

confidence: 99%

“…Expression of this form of LTP depends on presynaptic mechanisms (Staubli et al, 1990; Xiang et al, 1994; Weisskopf and Nicoll, 1995). Furthermore, LTD that is elicited by low-frequency stimulation (LFS), is preceded by potent facilitation of synaptic responses (called frequency facilitation) that is not seen at other hippocampal synapses (Salin et al, 1996; Toth et al, 2000; Moore et al, 2003; Hagena and Manahan-Vaughan, 2010). The role of mossy fiber (mf) plasticity in memory is unknown-however, the unique properties of frequency facilitation suggest it may play a role in working memory and/or informational integration.…”

Section: Introductionmentioning

confidence: 99%

Differentiation in the protein synthesis-dependency of persistent synaptic plasticity in mossy fiber and associational/commissural CA3 synapses in vivo

Hagena¹,

Manahan‐Vaughan²

2013

Front. Integr. Neurosci.

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Long-term potentiation (LTP) and long-term depression (LTD) are two mechanisms involved in the long-term storage of information in hippocampal synapses. In the hippocampal CA1 region, the late phases of LTP and LTD are protein-synthesis dependent. In the dentate gyrus, late-LTP but not LTD requires protein synthesis. The protein synthesis-dependency of persistent plasticity at CA3 synapses has not yet been characterized. Here, the roles of protein transcription and translation at mossy fiber (mf) and associational/commissural (AC)- synapses were studied in freely behaving rats. In control animals, low-frequency stimulation (LFS) evoked robust LTD (>24 h), whereas high-frequency stimulation (HFS) elicited robust LTP (>24 h) at both mf-CA3 and AC-CA3 synapses. Translation inhibitors prevented early and late phases of LTP and LTD at mf-CA3 synapses. In contrast, at AC–CA3 synapses, translation inhibitors prevented intermediate/late-LTP and late-LTD only. Transcription effects were also synapse-specific: whereas transcription inhibitors inhibited late-LTP and late-LTD (>3 h) at mf-CA3 synapses, at AC–CA3 synapses, protein transcription affected early-LTP and late-LTD. These results show that the AC-CA3 and mf-CA3 synapses display different properties in terms of their protein synthesis dependency, suggesting different roles in the processing of short- and long term synaptic plasticity.

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“…Previous studies demonstrated that application of the selective A1 receptor antagonist induced potent enhancement of mossy fiber response in vitro (Moore et al, 2003) and also in vivo (Klausnitzer and Manahan-Vaughan, 2008;Hagena and Manahan-Vaughan, 2010) by reducing tonic inhibitory effects of ambient adenosine. This effect is prominent at the mossy fiber synapse in comparison with adjacent associational-commissural synapse, and contributes, at least partly, to its characteristics such as low-release probability, large frequency facilitation and paired-pulse facilitation 4 (Nicoll and Schmitz, 2005).…”

mentioning

confidence: 99%

Assessing the roles of presynaptic ryanodine receptors and adenosine receptors in caffeine-induced enhancement of hippocampal mossy fiber transmission

Sato

Kamiya

2011

Neuroscience Research

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Caffeine robustly enhances transmitter release from the hippocampal mossy fiber terminals, although it remains uncertain whether calcium mobilization through presynaptic ryanodine receptors mediates this enhancement. In this study, we adopted a selective adenosine A1 blocker to assess relative contribution of A1 receptors and ryanodine receptors in caffeine-induced synaptic enhancement. Application of caffeine further enhanced transmission at the hippocampal mossy fiber synapse even after full blockade of adenosine A1 receptors. This result suggests that caffeine enhances mossy fiber synaptic transmission by two distinct presynaptic mechanisms, i.e. removal of A1 receptor-mediated tonic inhibition and ryanodine receptor-mediated calcium release from intracellular stores. (Onodera, 1973;Erulkar and Rahamimoff, 1978). Recently, much evidence has been accumulated for the presence of ryanodine-sensitive store in presynaptic terminals and/or axons at the hippocampal mossy fiber synapse onto CA3 pyramidal cell (Liang et al., 2002;Lauri et al., 2003;Sharma et al., 2003). This notion was also supported by the finding that application of caffeine, drug acting on ryanodine receptor channels to release Ca 2+ from intracellular stores, strongly enhanced synaptic transmission at the hippocampal mossy fiber synapse (Shimizu et al., 2008). This result also suggests the presence of functional ryanodine receptors and possible CICR mechanisms may be involved in robust activity-dependent presynaptic plasticity characteristic for this synapse.However, caffeine is also known to block adenosine A1 receptors potently (Fredholm et al., 1999). It was found that extracellular adenosine acts on presynaptic A1 receptors and suppresses transmitter release via activation of G i/o (Dunwiddie and Hoffer, 1980). Therefore, it remains to be determined whether activation of ryanodine receptors, in addition to blocking A1 receptors, mediates the caffeine-induced enhancement at this synapse. In this study, we addressed this issue using a selective blocker of A1 receptor (8-cyclopentyl-1,3-dipropylxanthine; DPCPX) and an inhibitor of ryanodine receptor channels (ryanodine). We found that caffeine enhanced the hippocampal mossy fiber response even under full blockade of A1 receptors, and that the magnitude of enhancement was decreased in the presence of ryanodine. We also measured presynaptic Ca 2+ levels within mossy fiber terminals by fluorescence recording during application of DPCPX and caffeine. A part of this work was presented elsewhere in an abstract form (Sato and Kamiya, 2009).All experiments were performed according to the guidelines for the care and use of

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Frequency Facilitation at Mossy Fiber-CA3 Synapses of Freely Behaving Rats Contributes to the Induction of Persistent LTD via an Adenosine-A1 Receptor-Regulated Mechanism

Cited by 32 publications

References 66 publications

The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing

The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing

Differentiation in the protein synthesis-dependency of persistent synaptic plasticity in mossy fiber and associational/commissural CA3 synapses in vivo

Assessing the roles of presynaptic ryanodine receptors and adenosine receptors in caffeine-induced enhancement of hippocampal mossy fiber transmission

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