Fimbrial control of bidirectional synaptic plasticity of medial perforant path‐dentate transmission

Nakao, Kazuhito; Ikegaya, Yuji; Yamada, Maki K.; Nishiyama, Nobuyoshi; Matsuki, Norio

doi:10.1002/syn.10168

Cited by 10 publications

(7 citation statements)

References 29 publications

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“…Based on lesions of the fimbria-fornix, Jas et al (2000) suggested that two independent DG-LTP modulatory pathways within the BLA-hippocampus system may exist (cf. Nakao et al, 2003), and Akirav and Richter-Levin (2002) found a ␤-adrenergic dependence on DG-LTP modulation by stimulating the ipsilateral but not the contralateral BLA, which also points to independent modulatory inputs.…”

Section: Discussionmentioning

confidence: 90%

Bidirectional Modulation of Hippocampal Long-Term Potentiation under Stress and No-Stress Conditions in Basolateral Amygdala-Lesioned and Intact Rats

Korz¹,

Frey²

2005

J. Neurosci.

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Hippocampal long-term potentiation (LTP) is widely considered as a cellular model for learning and memory formation. We have shown previously that protein synthesis-independent, early dentate gyrus (DG) LTP, lasting ϳ4 -5 h, can be transformed into a late-LTP with a duration of Ն24 h by a brief acute swim stress experience (high-stress condition). This reinforcement requires the activation of mineralocorticoid receptors and protein synthesis. The basolateral amygdala (BLA) is known to modulate glucocorticoid effects on the consolidation of spatial/contextual memory via a ␤-adrenergic mechanism. Interestingly, hippocampal DG-LTP can also be indirectly modulated by ␤-adrenergic and cholinergic/muscarinergic processes. Here, we show that the reinforcement of early-DG-LTP under high-stress conditions depends on the processing of novel spatial/contextual information. Furthermore, this reinforcement was blocked in BLA-lesioned animals compared with sham-operated and intact controls; however, it was not dependent on ␤-adrenergic or cholinergic/muscarinergic receptor activation. In contrast, under low-stress conditions, the induction of late-LTP in BLA-lesioned animals is facilitated, and this facilitation, again, was dependent on ␤-adrenergic activation. The data suggest that DG-LTP maintenance can be influenced by the BLA through different mechanisms: a short-lasting corticosterone-dependent and ␤-adrenergic-independent mechanism and a long-lasting mechanism that facilitated hippocampal ␤-adrenergic mechanisms.

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Section: Discussionmentioning

confidence: 90%

Bidirectional Modulation of Hippocampal Long-Term Potentiation under Stress and No-Stress Conditions in Basolateral Amygdala-Lesioned and Intact Rats

Korz¹,

Frey²

2005

J. Neurosci.

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“…By combining complex spike activity with theta rhythm, TBS approximates naturally occurring patterns of cell firing observed in the hippocampus and has been associated with widespread effects on synaptic efficiency and dynamic oscillation patterns (Diamond, ). Application of TBS to hippocampal afferent pathways produces robust and sustained long‐term potentiation (LTP) that is most effective in the theta range (i.e., 5 Hz, or 200 ms between pulses) (Nakao, ). LTP represents a long‐lasting increase in synaptic efficiency triggered by repetitive stimulation that produces postsynaptic Ca 2 + influx through N ‐methyl‐D‐aspartic acid (NMDA) glutamate receptors and, under some conditions, L‐type voltage‐gated Ca 2 + channels (Collingridge, ; Grover, ).…”

Section: Discussionmentioning

confidence: 99%

“…Other mechanisms may include dysregulated cellular homeostasis within the hippocampus (D'Ambrosio, ), dysfunctional synaptic neurotransmission (Toth, ; D'Ambrosio, ), regional changes in circuit excitability (Witgen, ), and a decrease in intrinsic hippocampal theta oscillations (Fedor, ). Disruption of the theta rhythm and synaptic function are particularly important because both have been implicated in the pathophysiology of memory loss (Winson, ; Nakao, ).…”

Section: Introductionmentioning

confidence: 99%

Improved learning and memory with theta‐burst stimulation of the fornix in rat model of traumatic brain injury

et al. 2014

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“…2 A (20,21). By changing the number of stimuli in each burst train, we find that LFBS, when delivered to the MPP, can produce varying levels of synaptic plasticity, i.e., a continuum from LTP to LTD, without any priming stimulation (Fig.…”

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confidence: 89%

Amygdala stimulation modulates hippocampal synaptic plasticity

Nakao

Matsuyama

Matsuki

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Experience-dependent synaptic plasticity is a fundamental feature of neural networks involved in the encoding of information, and the capability of synapses to express plasticity is itself activitydependent. Here, we introduce a ''low-frequency burst stimulation'' protocol, which can readily induce both long-term potentiation (LTP) and long-term depression (LTD) at in vivo medial perforant path-dentate gyrus synapses. By varying stimulation parameters, we were able to build a stimulus-response map of synaptic plasticity as a LTP-LTD continuum. The response curve displayed a bidirectional shift toward LTP and LTD, depending on the degree and timing of neural activity of the basolateral amygdala. The range of this plastic modulation was also modified by past activity of the basolateral amygdala, suggesting that the amygdala can arrange its ability to regulate the dentate plastic responses. The effects of the BLA activation were replicated by stimulation of the lateral perforant path and, hence, BLA stimulation may recruit the lateral entorhinal cortex. These results represent a high-order dimension of heterosynaptic modulations of hippocampal synaptic plasticity.BCM theory ͉ metaplasticity ͉ long-term potentiation ͉ long-term depression ͉ dentate gyrus T he amygdala plays an important role in emotional arousal and has emerged as a key modulator of memory storage in other brain regions (1, 2). Behavioral studies have indicated that microinjections of diverse pharmacological agents such as glucocorticoid-receptor agonists, ␤-adrenergic agents, amphetamine, and local anesthetics into the basolateral amygdala (BLA) enhance or impair hippocampus-dependent memory (3-7).In support of these studies, we and other groups have reported that BLA activation͞inactivation or delivery of glutamatergic and ␤-adrenergic agents into the BLA can modulate long-term potentiation (LTP) at the medial perforant path (MPP)-dentate gyrus (DG) synapses in the hippocampal formation (8-13). Prior stimulation of the BLA is also capable of gating subsequent induction of LTP in the DG (14, 15). The BLA modulation of hippocampal LTP is, therefore, a compelling candidate mechanism underlying the amygdalar control of the hippocampal memory system.In this respect, however, several issues remain to be resolved. For example, it is uncertain which brain region relays BLA inputs to the DG, which dentate substratum ultimately receives the BLA input, whether the BLA also modulates hippocampal long-term depression (LTD), or how various patterns of BLA activity alter its ability to modulate DG plasticity. In particular, the last two questions have been difficult to address because there is no simple experimental system that can reliably induce homosynaptic LTD in vivo; note that, unlike the case of slice preparations, in vivo LTD is usually inducible only when the synapses are electrically or pharmacologically primed before a LTD-inducing stimulus (16)(17)(18)(19).In the present work, we describe an in vivo protocol of low-frequency burst stimulation (LFBS),...

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Fimbrial control of bidirectional synaptic plasticity of medial perforant path‐dentate transmission

Cited by 10 publications

References 29 publications

Bidirectional Modulation of Hippocampal Long-Term Potentiation under Stress and No-Stress Conditions in Basolateral Amygdala-Lesioned and Intact Rats

Bidirectional Modulation of Hippocampal Long-Term Potentiation under Stress and No-Stress Conditions in Basolateral Amygdala-Lesioned and Intact Rats

Improved learning and memory with theta‐burst stimulation of the fornix in rat model of traumatic brain injury

Amygdala stimulation modulates hippocampal synaptic plasticity

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