Naloxone blocks the induction of long-term potentiation in the lateral but not in the medial perforant pathway in the anesthetized rat

doi:10.1016/0006-8993(88)91052-9

Brain Research

Volume 449, Issues 1–2, 24 May 1988, Pages 352-356

https://doi.org/10.1016/0006-8993(88)91052-9 Get rights and content

Abstract

The possible importance of opioid peptides in the induction of long-term potentiation (LTP) was investigated in the perforant pathgranule cell system. A high-frequency train (400 Hz) was delivered to the lateral or medial perforant path, during push-pull perfusion of the dentate molecular layer with artificial cerebrospinal fluid (CSF) alone, or with CSF containing naloxone (10⁻⁴ M). Naloxone effectively blocked the induction, but not the maintenance of LTP in the lateral perforant path, a putative proenkephalin system. Naloxone did not affect the production of LTP in the medial pathway. These findings suggest that activation of naloxone-sensitive receptors is necessary for the full expression of LTP in the lateral perforant pathway.

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The effects of opioid receptor antagonists on LTP induction may be understood from current views of the actions of opioid receptors in the hippocampus. Previous studies indicate LTP induction at lateral perforant path-dentate gyrus synapses is blocked by μ opioid receptor antagonists (Bramham & Sarvey, 1996; Xie & Lewis, 1991, 1995; Bramham et al., 1988). In addition, it is well established that μ opioid receptor agonists can inhibit both GABAergic interneurons (Madison & Nicoll, 1988) and GABA release in hippocampal interneurons (Cohen, Doze, & Madison, 1992), resulting in the excitation of hippocampal principal neurons due to a reduction in GABAergic inhibition (Corrigall, 1983).
The medial and lateral perforant path projections to the hippocampal CA3 region display distinct mechanisms of long-term potentiation (LTP) induction, N-methyl-d-aspartate (NMDA) and opioid receptor dependent, respectively. However, medial and lateral perforant path projections to the CA3 region display associative LTP with coactivation, suggesting that while they differ in receptors involved in LTP induction they may share common downstream mechanisms of LTP induction. Here we address this interaction of LTP induction mechanisms by evaluating the contribution of opioid receptors to the induction of associative LTP among the medial and lateral perforant path projections to the CA3 region in vivo. Local application of the opioid receptor antagonists naloxone or Cys2-Tyr3-Orn5-Pen7-amide (CTOP) normally block induction of lateral perforant path-CA3 LTP. However, these opioid receptor antagonists failed to block associative LTP in lateral perforant path-CA3 synapses when it was induced by strong coactivation of the medial perforant pathway which displays NMDAR-dependent LTP. Thus strong activation of non-opioidergic afferents can substitute for the opioid receptor activation required for lateral perforant path LTP induction. Conversely, medial perforant path-CA3 associative LTP was blocked by opioid receptor antagonists when induced by strong coactivation of the opioidergic lateral perforant path. These data indicate endogenous opioid peptides contribute to associative LTP at coactive synapses when induced by strong coactivation of an opioidergic afferent system. These data further suggest that associative LTP induction is regulated by the receptor mechanisms of the strongly stimulated pathway. Thus, while medial and lateral perforant path synapses differ in their mechanisms of LTP induction, associative LTP at these synapses share common downstream mechanisms of induction.
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High-frequency stimulation of lateral perforant path is accompanied by a heterosynaptic long-term depression (LTD) of medial perforant path synaptic responses in both the dentate gyrus and the CA3 region of the hippocampus. We reported previously that LTP induction at lateral perforant path-CA3 synapses is unaffected by NMDA antagonists. However, it is not known if heterosynaptic LTD that is observed in the CA3 region following lateral perforant path stimulation also is independent from NMDA receptors. We address this question in anesthetized adult rats using systemic administration of the competitive NMDA receptor antagonist CPP. Induction of lateral perforant path-CA3 LTP produced a sustained heterosynaptic depression of medial perforant path-CA3 responses. Systemic administration of CPP (10 mg/kg) was ineffective in blocking the induction of LTP at lateral perforant path-CA3 responses. However, heterosynaptic LTD of medial perforant path-CA3 responses was blocked completely by CPP. These data indicate that NMDA receptors are not required for the induction of lateral perforant path-CA3 LTP, but are involved in the induction of heterosynaptic LTD that accompanies lateral perforant path activity. The requirement for NMDA receptors for heterosynaptic LTD suggests one functional role of NMDA receptors at termination fields of the lateral perforant path.

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^☆: A preliminary account of this work has been reported.

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Short communicationNaloxone blocks the induction of long-term potentiation in the lateral but not in the medial perforant pathway in the anesthetized rat☆

Abstract

Eur. J. Pharmacol.

Brain Research

Trends Neurosci.

Neuroscience

J. Neurosci. Meth.

Brain Research

Brain Research

Neurosci. Lett.

Brain Research

Neurosci. Lett.

Neurosci. Lett.

Neuropeptides

Brain Research

Prog. Brain Res.

Prog. Brain Res.

Brain Research

Short communication
Naloxone blocks the induction of long-term potentiation in the lateral but not in the medial perforant pathway in the anesthetized rat☆