» Articles » PMID: 22041183

Heterosynaptic Long-term Potentiation at Interneuron-principal Neuron Synapses in the Amygdala Requires Nitric Oxide Signalling

Overview
Journal J Physiol
Specialty Physiology
Date 2011 Nov 2
PMID 22041183
Citations 32
Authors
Affiliations
Soon will be listed here.
Abstract

Long-lasting changes of synaptic efficacy are thought to be a prerequisite for memory formation and maintenance. In the basolateral complex of the amygdala (BLA), one of the main regions for fear and extinction learning of the brain, various forms of long-term potentiation (LTP) have been described for excitatory glutamatergic synapses. In contrast, little is known about the mechanisms of LTP at inhibitory GABAergic synapses. Here we provide evidence that (1) LTP at inhibitory GABAergic synapses (LTP(i)) between inhibitory interneurons and principal neurons (PNs) can be induced by theta-burst stimulation (TBS), (2) this LTP(i) is prevented by AMPA- or NMDA-receptor antagonists, and (3) this LTP(i) is abolished by the NO synthase (NOS) inhibitor L-NAME or the NO scavenger PTIO, and thus is critically dependent on nitric oxide (NO) signalling. These findings are corroborated by immunocytochemical stainings for neuronal (n) NOS, which revealed the existence of nNOS-positive neurons and fibres in the BLA. We conclude that LTP of GABAergic synaptic transmission to PNs is induced by activation of AMPA and NMDA receptors at glutamatergic synapses and subsequent retrograde NO signalling to enhance GABAergic transmission. This form of LTP at GABAergic synapses comprises a novel form of heterosynaptic plasticity within the BLA, apt to shape conditioned fear responses.

Citing Articles

The Neural Palette of Heme: Altered Heme Homeostasis Underlies Defective Neurotransmission, Increased Oxidative Stress, and Disease Pathogenesis.

Soladogun A, Zhang L Antioxidants (Basel). 2025; 13(12.

PMID: 39765770 PMC: 11672823. DOI: 10.3390/antiox13121441.


Cholecystokinin-expressing interneurons mediated inhibitory transmission and plasticity in basolateral amygdala modulate stress-induced anxiety-like behaviors in mice.

Fang W, Chen X, He J Neurobiol Stress. 2024; 33:100680.

PMID: 39502835 PMC: 11536064. DOI: 10.1016/j.ynstr.2024.100680.


Heterosynaptic plasticity-induced modulation of synapses.

Kourosh-Arami M, Komaki A, Gholami M, Marashi S, Hejazi S J Physiol Sci. 2023; 73(1):33.

PMID: 38057729 PMC: 10717068. DOI: 10.1186/s12576-023-00893-1.


The Basolateral Amygdala: The Core of a Network for Threat Conditioning, Extinction, and Second-Order Threat Conditioning.

Sepahvand T, Power K, Qin T, Yuan Q Biology (Basel). 2023; 12(10).

PMID: 37886984 PMC: 10604397. DOI: 10.3390/biology12101274.


Olfactory threat extinction in the piriform cortex: An age-dependent employment of NMDA receptor-dependent long-term depression.

Sepahvand T, Nazari N, Qin T, Rajani V, Yuan Q Proc Natl Acad Sci U S A. 2023; 120(44):e2309986120.

PMID: 37878718 PMC: 10622944. DOI: 10.1073/pnas.2309986120.


References
1.
Ota K, Pierre V, Ploski J, Queen K, Schafe G . The NO-cGMP-PKG signaling pathway regulates synaptic plasticity and fear memory consolidation in the lateral amygdala via activation of ERK/MAP kinase. Learn Mem. 2008; 15(10):792-805. PMC: 2632793. DOI: 10.1101/lm.1114808. View

2.
Ota K, Monsey M, Wu M, Schafe G . Synaptic plasticity and NO-cGMP-PKG signaling regulate pre- and postsynaptic alterations at rat lateral amygdala synapses following fear conditioning. PLoS One. 2010; 5(6):e11236. PMC: 2888610. DOI: 10.1371/journal.pone.0011236. View

3.
Pape H, Pare D . Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev. 2010; 90(2):419-63. PMC: 2856122. DOI: 10.1152/physrev.00037.2009. View

4.
Spampanato J, Polepalli J, Sah P . Interneurons in the basolateral amygdala. Neuropharmacology. 2010; 60(5):765-73. DOI: 10.1016/j.neuropharm.2010.11.006. View

5.
Nugent F, Niehaus J, Kauer J . PKG and PKA signaling in LTP at GABAergic synapses. Neuropsychopharmacology. 2009; 34(7):1829-42. PMC: 2680921. DOI: 10.1038/npp.2009.5. View