Nitric Oxide Signaling Exerts Bidirectional Effects on Plasticity Inductions in Amygdala

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Shin, Ryong Moon ^a   Higuchi, Makoto ^a   Suhara, Tetsuya ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONDITIONING; CONTROLLED STUDY; FEAR; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); CYCLIC GMP; DIFFUSION; FEAR; LONG-TERM POTENTIATION; MALE; MEMORY; NEURONAL PLASTICITY; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SYNAPSES; THALAMUS;

EID: 84884581872     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074668     Document Type: Article

References (47)

1. Casado M, Isope P, Ascher P, (2002) Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron 33: 123-130. doi:10.1016/S0896-6273(01)00568-2. PubMed: 11779485.
2. Jacoby S, Sims RE, Hartell NA, (2001) Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices. J Physiol 535: 825-839. doi:10.1111/j.1469-7793.2001.t01-1-00825.x. PubMed: 11559778.
3. Schuman EM, Madison DV, (1994) Locally distributed synaptic potentiation in the hippocampus. Science 263: 532-536. doi:10.1126/science.8290963. PubMed: 8290963.
4. Sequeira SM, Malva JO, Carvalho AP, Carvalho CM, (2001) Presynaptic N-methyl-D-aspartate receptor activation inhibits neurotransmitter release through nitric oxide formation in rat hippocampal nerve terminals. Mol Brain Res 89: 111-118. doi:10.1016/S0169-328X(01)00069-9. PubMed: 11311981.
5. Morris JS, Ohman A, Dolan RJ, (1999) A subcortical pathway to the right amygdale mediating "unseen" fear. Proc Natl Acad Sci U S A 96: 1680-1685. doi:10.1073/pnas.96.4.1680. PubMed: 9990084.
6. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM, (1990) The Lateral amygdaloid Nucleus: Sensory interface of the amygdala in fear conditioning. J Neurosci 10: 1062-1069. PubMed: 2329367.
7. McKernan MG, Shinnick-Gallagher P, (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390: 607-611. doi:10.1038/37605. PubMed: 9403689.
8. Rogan MT, Stäubli UV, LeDoux JE, (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390: 604-607. doi:10.1038/37601. PubMed: 9403688.
9. Miserendino MJD, Sananes CB, Melia KR, Davis M, (1991) Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716-718.
10. Shumyatsky GP, Malleret G, Shin RM, Takizawa S, Tully K, et al. (2002) Stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123: 697-709. PubMed: 16286011.
11. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY, (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34: 289-300. doi:10.1016/S0896-6273(02)00645-1. PubMed: 11970870.
12. Ota KT, Pierre VJ, Ploski JE, Queen K, Schafe GE, (2008) 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 15: 792-805. doi:10.1101/lm.1114808. PubMed: 18832566.
13. Schafe GE, Bauer EP, Rosis S, Farb CR, Rodrigues SM, et al. (2005) Memory consolidation of pavlovian fear conditioning requires nitric oxide signaling in the lateral amygdala. Eur J Neurosci 22: 201-211. doi:10.1111/j.1460-9568.2005.04209.x. PubMed: 16029210.
14. Paul C, Schöberl F, Weinmeister P, Micale V, Wotjak CT, et al. (2008) Signaling through cGMP-dependent protein kinase I in the amygdala is critical for auditory-cued fear memory and long-term potentiation. J Neurosci 28: 8310-8317. PubMed: 19109502.
15. Watanabe Y, Saito H, Abe K, (1995) Nitric oxide is involved in long-term potentiation in the medial but not lateral amygdala neurons synapses in vitro. Brain Res 688: 233-236. doi:10.1016/0006-8993(95)00563-6. PubMed: 8542316.
16. Shin RM, Tully K, Li Y, Cho JH, Higuchi M, et al. (2010) Hierarchical order of coexisting pre- and postsynaptic forms of long-term potentiation at synapses in amygdala. Proc Natl Acad Sci U S A 107: 19073-19078. doi:10.1073/pnas.1009803107. PubMed: 20956319.
17. Cho JH, Bayazitov IT, Meloni EG, Myers KM, Carlezon WA Jr,. et al. (2011) Coactivation of thalamic and cortical pathways induceds input timing-dependent plasticity in amygdala. Nat Neurosci 15: 113-122. doi:10.1038/nn.2993. PubMed: 22158512.
18. Shin RM, Tsvetkov E, Bolshakov VY, (2006) Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways. Neuron 52: 883-896. doi:10.1016/j.neuron.2006.10.010. PubMed: 17145508.
19. Tsvetkov E, Shin RM, Bolshakov VY, (2004) Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 41: 139-151. doi:10.1016/S0896-6273(03)00800-6. PubMed: 14715141.
20. Bender VA, Bender KJ, Brasier DJ, Feldman DE, (2006) Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26: 4166-4177. doi:10.1523/JNEUROSCI.0176-06.2006. PubMed: 16624937.
21. Corlew R, Wang Y, Ghermazien H, Erisir A, Philpot BD, (2007) Developmental switch in the conrtribution of presynaptic and postsynaptic NMDA receptors to long-term depression. J Neurosci 27: 9835-9845. doi:10.1523/JNEUROSCI.5494-06.2007. PubMed: 17855598.
22. Li H, Chen A, Xing G, Wei ML, Rogawski MA, (2001) Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 4: 612-620. doi:10.1038/88432. PubMed: 11369942.
23. Izumi Y, Clifford DB, Zorumski CF, (1992) Inhibition of long-term potentiation by NMDA-mediated nitric oxide release. Science 257: 1273-1278. doi:10.1126/science.1519065. PubMed: 1519065.
24. Feil R, Hofmann F, Kleppisch T, (2005) Function of cGMP-dependent protein kinases in the nervous system. Rev Neurosci 16: 23-41. PubMed: 15810652.
25. Humeau Y, Herry C, Kemp N, Shaban H, (2005) Dendritic spine heterogeneity determines afferent-specificnhebbian plasticity in the amygdale. Neuron 45: 119-131. doi:10.1016/j.neuron.2004.12.019. PubMed: 15629707.
26. Zucker RS, (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31. doi:10.1146/annurev.ne.12.030189.000305. PubMed: 2648947.
27. Burnashev N, Villarroel A, Sakmann B, (1996) Dimensiona and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence of Q/R site residues. J Physiol 496: 165-173. PubMed: 8910205.
28. Humeau Y, Shaban H, Bissière S, Lüthi A, (2003) Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature 426: 841-845. doi:10.1038/nature02194. PubMed: 14685239.
29. Humeau Y, Reisel D, Johnson AW, Borchardt T, Jensen V, et al. (2007) A pathway-specific function for different AMPA receptor subunits in amygdala long-term Potentiation and fear conditioning. J Neurosci 27: 10947-10956. doi:10.1523/JNEUROSCI.2603-07.2007. PubMed: 17928436.
30. Rumpel S, LeDoux JE, Zador A, Malinow R, (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308: 83-88. doi:10.1126/science.1103944. PubMed: 15746389.
31. Quirk GJ, Armony JL, LeDoux JE, (1995) Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19: 613-624. PubMed: 9331352.
32. Romanski LM, LeDoux JE, (1992) Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J Neurosci 21: 4501-4509. PubMed: 1331362.
33. Campeau S, Davis M, (1995) Involvement of subcortical and cortical afferents to the lateral nucleus the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15: 2312-2327. PubMed: 7891169.
34. Doyère V, Schafe GE, Sigurdsson T, LeDoux JE, (2003) Long-term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala. Eur J Neurosci 17: 2701-2715. PubMed: 12823477.
35. Lang EJ, Paré D, (1997) Similar inhibitory processes dominate the responses at cat lateral amygdaloid projection neurons to their various afferents. J Neurophysiol 77: 341-352. PubMed: 9120575.
36. Li XF, Armony JL, LeDoux JE, (1996) GABAA and GABAB receptors differentially regulate synaptic transmission in the auditory thalamo-amygdala pathway: an in vivo microiontophoretic study and a model. Synapse 24: 115-124. doi:10.1002/(SICI)1098-2396(199610)24:2. PubMed: 8890453.
37. Sugita S, Tanaka E, North RA, (1997) Membrance properties and synaptic potentials of three types of neurone on rat lateral amygdala. J Physiol 460: 705-718.
38. Bissière S, Humeau Y, Lüthi A, (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6: 587-592. doi:10.1038/nn1058. PubMed: 12740581.
39. Kodirov SA, Takizawa S, Joseph J, Kandel ER, Shumyatsky GP, et al. (2006) Synaptically relerased zinc gates long-term potentiation in fear conditioning pathways. Proc Natl Acad Sci U S A 103: 15218-15223. doi:10.1073/pnas.0607131103. PubMed: 17005717.
40. Tully K, Li Y, Tsvetkov E, Bolshakov VY, (2007) Norepinephrine enables the induction of associative long-term potentiation in the thalamo-amygdala synapse. Proc Natl Acad Sci U S A 104: 14146-14150. doi:10.1073/pnas.0704621104. PubMed: 17709755.
41. Johansen JP, Hamanaka H, Monfils MH, Behnia R, Deisseroth K, et al. (2010) Optical activation of lateral amygdala pyramidal cells instructs associative fear learning. Proc Natl Acad Sci U S A 107: 12692-12697. doi:10.1073/pnas.1002418107. PubMed: 20615999.
42. Quirk GJ, Repa C, LeDoux JE, (1997) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recording in the freely behaving rat. Neuron 15: 1029-1039.
43. Sato T, Suzuki E, Yokoyama M, Watanabe S, Miyaoka H, (2005) Auditory fear conditioning and conditioned stress raise NO3 level in the amygdala. Neuropsychobiology 53: 142-147.
44. Huang YY, Colino A, Selig DK, Malenka RC, (1992) The influence of prior synaptic activity on the induction of long-term potentiation. Science 255: 730-733. doi:10.1126/science.1346729. PubMed: 1346729.
45. Garthwaite J, Boulton CL, (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57: 683-706. doi:10.1146/annurev.ph.57.030195.003343. PubMed: 7539993.
46. Ahmed MS, Siegelbaum SA, (2009) Recruitment of N-type Ca2+ channels during LTP enhances low release efficacy of hippocampal CA1 perforant path synapses. Neuron 63: 372-385. doi:10.1016/j.neuron.2009.07.013. PubMed: 19679076.
47. Fourcaudot E, Gambino F, Casassus G, Poulain B, Humeau Y, et al. (2009) L-type voltage-dependent Ca2+ channels mediate expression of presynaptic LTP in amygdala. Nat Neurosci 12: 1093-1095.