Persistent (&gt;24h) long-term depression in the dentate gyrus of freely moving rats is not dependent on activation of NMDA receptors, L-type voltage-gated calcium channels or protein synthesis

Poschel, B. P. H.; Manahan‐Vaughan, Denise

doi:10.1016/j.neuropharm.2006.07.019

Cited by 32 publications

(35 citation statements)

References 53 publications

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“…The bars in B, D, and E represent the time period in which myr-ZIP was applied. Other abbreviations and symbols are as in Figure 1. can be induced in the apical dendrites of CA1 pyramidal neurons under distinct circumstances (Kemp et al, 2000;ManahanVaughan, 2000;Manahan-Vaughan et al, 2000;Frey, 2003, 2004;Malenka and Bear, 2004;Pöschel and Manahan-Vaughan, 2007). Here, we clearly demonstrate that longer-lasting forms of LTD can only be induced in the distal part of the apical dendrites of CA1 pyramidal neurons.…”

Section: Discussionsupporting

confidence: 50%

“…Long-term potentiation (LTP; prolonged increase in synaptic efficacy after brief high-frequency trains of afferent fibers) as well as long-term depression (LTD; prolonged decrease in synaptic efficacy in response to low-frequency stimulation patterns to afferent fibers) can be induced in this region. We refer here only to NMDA receptordependent forms, which can express under distinct circumstances a protein synthesis-independent early-stage (E-LTD or E-LTP, Ͻ4 h) and a protein synthesis-dependent late phase (L-LTD or L-LTP, Ͼ4 h), although various forms of LTP and LTD exist (for review, see Massey and Bashir, 2007;Sajikumar et al, 2005a;Pöschel and Manahan-Vaughan, 2007;Frey and Frey, 2008). It is also well documented that long-lasting forms of LTP can be induced in several parts of the apical CA1 dendrite, regardless of whether it is studied at proximal or distal sites (Frey and Morris, 1997).…”

Section: Introductionmentioning

confidence: 99%

“…However, less is known about forms of LTD expression at different parts of apical CA1 dendrites. The cellular mechanisms for the induction and expression of LTD (as well as LTP) can vary depending on the stimulation protocol, brain subregion, and stage of development (Kemp et al, 2000;Malenka and Bear, 2004;Pöschel and Manahan-Vaughan, 2007). Prolonged low-frequency stimulation (LFS) is required to induce a prolonged protein synthesis-dependent L-LTD, which also requires NMDA receptor activation, postsynaptic Ca 2ϩ influx, and activation of a serine/threonine phosphatase cascade (Mulkey et al, 1994;Manahan-Vaughan et al, 2000;Sajikumar and Frey, 2003;Sajikumar et al, 2005a).…”

Section: Introductionmentioning

confidence: 99%

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Functional Differences between and across Different Regions of the Apical Branch of Hippocampal CA1 Dendrites with Respect to Long-Term Depression Induction and Synaptic Cross-Tagging

Parvez¹,

Ramachandran²,

Frey³

2010

J. Neurosci.

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The hippocampus is an ideal system to study synaptic plasticity in the context of learning and memory. The induction, expression, and interaction of long-term potentiation (LTP) as well as long-term depression (LTD) are essential elements for the functioning of complex networks in information processing and storage. Here we investigated whether different loci at the apical dendritic branch of CA1 pyramidal neurons are characterized by different capabilities to induce, express, and interact with LTP and LTD in hippocampal slices in vitro. We found that high-frequency stimulation resulted in longer-lasting forms of LTP in proximal and distal parts of the apical dendrites, whereas low-frequency stimulation induced longer-lasting LTD in distal but not at proximal parts. Interestingly, processes of "synaptic cross-tagging" could be described for any form of LTP transformation from early-stage LTP (E-LTP) into late-phase LTP (L-LTP) in distal and proximal parts, but for LTD, only at the distal part but not for the proximal part, although low-frequency stimulation at the proximal input, which resulted here only in a short-term depression, was paradoxically able to reinforce E-LTP into L-LTP at distal parts. We have identified protein kinase Mzeta (PKMzeta) as the LTP-specific, synthesized plasticity-related protein transforming E-LTP into L-LTP by strong low-frequency stimulation in the apical CA dendrite by cross-tagging mechanisms.

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Section: Discussionsupporting

confidence: 50%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Functional Differences between and across Different Regions of the Apical Branch of Hippocampal CA1 Dendrites with Respect to Long-Term Depression Induction and Synaptic Cross-Tagging

Parvez¹,

Ramachandran²,

Frey³

2010

J. Neurosci.

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“…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%

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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“…Furthermore, different hippocampal subregions respond with distinct types of synaptic plasticity to novel spatial experience (Kemp and Manahan-Vaughan 2008a). LTD in the dentate gyrus and CA1 regions of freely behaving rats is typically induced by 1 Hz low-frequency stimulation (LFS) although these forms of synaptic plasticity do not share the same induction mechanisms (Dudek and Bear 1992; Mulkey et al 1993, 1994; O'Mara et al 1995; Manahan-Vaughan 1997; Wang et al 1998; Pöschel and Manahan-Vaughan 2005, 2007). Typical studies of FF involve applying stimuli for 30–150 s (Salin et al 1996; Dobrunz and Stevens 1999; Toth et al 2000; Klausnitzer and Manahan-Vaughan 2008).…”

Section: Introductionmentioning

confidence: 99%

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

Manahan‐Vaughan

2009

Cerebral Cortex

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Frequency facilitation (FF), comprising a rapid and multiple-fold increase in the magnitude of evoked field potentials, is elicited by low-frequency stimulation (LFS) at mossy fiber–CA3 synapses. Here, we show that in freely behaving rats, FF reliably occurs in response to 1 and 2Hz but not in response to 0.25-, 0.3-, or 0.5-Hz LFS. Strikingly, prolonged (∼600 s) FF was tightly correlated to the induction of long-term depression (LTD) in freely moving animals. Although LFS at 2 Hz elicited unstable FF and unstable LTD, application of LFS at 1 Hz elicited pronounced FF, as well as robust LTD that persisted for over 24 h. This correlation of prolonged FF with LTD was absent at stimulation frequencies that did not induce FF. The adenosine-A1 receptor appears to participate in these effects: Application of adenosine-A1, but not adenosine-A3, receptor antagonists enhanced mossy fiber synaptic transmission and occluded FF. Furthermore, adenosine-A1 receptor antagonism resulted in more stable FF at 1 or 2 Hz and elicited more potent LTD. These data support the fact that FF contributes to the enablement of long-term information storage at mossy fiber–CA3 synapses and that the adenosine-A1 receptor may regulate the thresholds for this process.

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Persistent (>24h) long-term depression in the dentate gyrus of freely moving rats is not dependent on activation of NMDA receptors, L-type voltage-gated calcium channels or protein synthesis

Cited by 32 publications

References 53 publications

Functional Differences between and across Different Regions of the Apical Branch of Hippocampal CA1 Dendrites with Respect to Long-Term Depression Induction and Synaptic Cross-Tagging

Functional Differences between and across Different Regions of the Apical Branch of Hippocampal CA1 Dendrites with Respect to Long-Term Depression Induction and Synaptic Cross-Tagging

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

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

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