Synaptic modulation via basolateral amygdala on the rat hippocampus-medial prefrontal cortex pathway in fear extinction

Journal of Pharmacological Sciences

Volumn 123, Issue 3, 2013, Pages 267-278

  Inoue, Sumitaka ^a   Kamiyama, Hidekazu ^a   Matsumoto, Machiko ^a   Yanagawa, Yoshiki ^a   Hiraide, Sachiko ^a   Saito, Yasuhiro ^a   Shimamura, Kei Ichi ^a   Togashi, Hiroko ^a  

^a HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

Author keywords

Basolateral amygdala; Extinction retrieval; Low frequency stimulation; Medial prefrontal cortex; Synaptic potentiation

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL AMYGDALA; BRAIN FUNCTION; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; DENTATE GYRUS; FEAR; HIPPOCAMPUS; LATENT PERIOD; LONG TERM EXPOSURE; LONG TERM POTENTIATION; MALE; MEDIAL PREFRONTAL CORTEX; NEUROMODULATION; NONHUMAN; PREFRONTAL CORTEX; RAT; RECALL; REINFORCEMENT; SYNAPTIC TRANSMISSION;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); DIZOCILPINE MALEATE; ELECTRIC STIMULATION; EVOKED POTENTIALS; EXTINCTION, PSYCHOLOGICAL; FEAR; HIPPOCAMPUS; HUMANS; HYDROCARBONS, CHLORINATED; LONG-TERM POTENTIATION; MALE; MODELS, ANIMAL; PARAHIPPOCAMPAL GYRUS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; STRESS, PSYCHOLOGICAL; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84890491693     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.13123FP     Document Type: Article

References (48)

1. Abraham WC, Bear NF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996;19:126-130.
2. Abraham WC. Metaplasticity: tuning synapses and networks for plasticity. Nature Reviews Neurosci. 2008;9:387-399.
3. Shors TG, Gallegos RA, Breindl A. Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse. 1997;26:209-217.
4. Shakesby AC, Anwyl R, Rowan MJ. Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: rapid actions of serotonergic and antidepressant agents. J Neurosci. 2002;22:3638-3644.
5. Kavushansky A, Vouimba R-M, Cohen H, Richter-Levin G. Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus. 2006;16:35-42.
6. Spyrka J, Hess G. Repeated restraint-induced modulation of long-term potentiation in the dentate gyrus of the mouse. Brain Res. 2010;1320:28-33.
7. Vouimba R-M, Richter-Levin G. Physiological dissociation in hippocampal subregions in response to amygdala stimulation. Cereb Cortex. 2005;15:1815-1821.
8. Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci. 2001;21:3697-3703.
9. Vouimba R-M, Yaniv D, Diamond D, Richter-Levin G. Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur J Neurosci. 2004;19:1887-1894.
10. Kim JJ, Lee HJ, Han J-S, Packard MG. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci. 2001;21:5222-5228.
11. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol. 1999;403:229-260.
12. Bacon SJ, Headlam AJN, Gabbott PLA, Smith AD. Amygdala input to medial prefrontal cortex (mPFC) in the rat: a light and electron microscope study. Brain Res. 1996;720:211-219.
13. Cardinal RN, Parkinson JA, Hall J, Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum and prefrontal cortex. Neurosci Biobehav Rev. 2002;26:321-352.
14. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci. 2002;5:844-852.
15. Myers KM, Davis M. Mechanisms of fear extinction. Mol Psychiatry. 2007;12:120-150.
16. Quirk GJ, Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology. 2008;33:56-72.
17. Godsil BP, Kiss JP, Spedding M, Jay TM. The hipppocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur Neuropsychopharmacol. 2013;23:1165-1181.
18. Richter-Levin G, Maroun M. Stress and amygdala suppression of metaplasticity in the medial prefrontal cortex. Cereb Cortex. 2010;20:2433-2441.
19. Kim JJ, Koo JW, Lee HJ, Han J-S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J Neurosci. 2005;35:1532-1539.
20. Hirata R, Matsumoto M, Judo C, Yamaguchi T, Izumi T, Yoshioka M, et al. Possible relationship between the stress-induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats. Synapse. 2009;63:549-556.
21. Ziabreva I, Poeggel G, Schnabel R, Braun K. Separaion-induced receptorchanges in the hippocampus and amygdala of octodon degus:influence f maternal vocalizations. J Neurosci. 2003;23:5329-5366.
22. Blaise JH, Koranda JL, Chow U, Haines KE, Dorward EC. Neonatal isolation stress alters bidirectional long-term synaptic plasticity in amygdalo-hippocampal synapses in freely behaving adult rats. Brain Res. 2008;1193:25-33.
23. Matsumoto M, Togashi H, Konno K, Koseki H, Hirata R, Izumi T, et al. Early postnatal stress alters the extinction of context-dependent conditioned fear in adult rats. Pharmacol Biochem Behav. 2008;89:247-252.
24. Judo C, Matsumoto M, Yamazaki D, Hiraide S, Yanagawa Y, Kimura S, et al. Early stress exposure impairs synaptic potentiation in the rat medial prefrontal cortex underlying contextual fear extinction. Neuroscience. 2010;169:1705-1714.
25. Koseki H, Matsumoto M, Togashi H, Miura Y, Fukushima K, Yoshioka M. Alteration of synaptic transmission in the hippo-campal-mPFC pathway during extinction trials of context-dependent fear memory in juvenile rat stress models. Synapse. 2009;63:805-813.
26. Jay TM, Burette F, Laroche S. NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat. Eur J Neurosci. 1995;7:247-250.
27. Hugus S, Garcia R. Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn Mem. 2007;14;520-524.
28. Naie K, Manahan-Vaughan D. Regulation by metabotropic glutamate receptor 5 of LTP in the dentate gyrus of freely moving rats: relevance for learning and memory formation. Cereb Cortex. 2004;14:189-198.
29. Fanselow MS. Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci. 1980;15:177-182.
30. Mockett B, Coussens C, Abraham WC. NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation. Eur J Neurosci. 2002;15:1819-1826.
31. MacDonald JF, Jackson MF, Beazely MA. G protein-coupled receptors control NMDARs and metaplasticity in the hippocampus. Biochim Biophys Acta. 2007;1768:941-951.
32. Vouimba R-M, Richter-Levin G. Different patterns of amygdala priming differentially affect dentate gyrus plasticity and corticosterone, but not CA1 plasticity. Front Neural Circuits. 2013; 7:1-10.
33. Matsumoto M, Tachibana K, Togashi H, Tahara K, Kojima T, Yamaguchi T, et al. Chronic treatment with milnacipran reverses the impairment of synaptic plasticity induced by conditioned fear stress. Psychopharmacology. 2005;179:606-612.
34. Hirata R, Togashi H, Matsumoto M, Yamaguchi T, Izumi T, Yoshioka M. Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats. Brain Res. 2008;1226:27-32.
35. Zelcer I, Cohen H, Richter-Levin G, Lebiosn T, Grossberger T, Barkai E. Cellular correlate of learning-induced metaplasticity in the hippocampus. Cereb Cortex. 2006;16:460-468.
36. Jay TM, Thierry AM, Wiklund L, Glowinski J. Excitatory aminoacid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission. Eur J Neurosci. 1992;4:1285-1295.
37. Ji J, Maren S. Hippocampal involvement in contextual modulation of fear extinction. Hippocamppus. 2007;17:749-758.
38. Saito Y, Matsumoto M, Otani S, Yanagawa Y, Sachiko Hiraide S, Ishikawa S, et al. Phase-dependent synaptic changes in the hippocampal CA1 field underlying extinction processes in freely moving rats. Neurobiol Learn Mem. 2012;97:361-369.
39. Quirk GJ, Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology. 2008;33:56-72.
40. Herry C, Garcia R. Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci. 2002;22:577-583.
41. Richardson R, Ledgerwood L, Cranney J. Facilitation of fear extinction by D-cycloserine: theoretical and clinical implications. Learn Mem. 2004;11:510-516.
42. Davis M, Ressler K, Rothbaum BO, Richardson R. Effects of D-cycloserine on extinction: translation from preclinical to clinical work. Biol Psychiatry. 2006;60:369-375.
43. Mao S-C, Hsiao Y-H, Gean P-W. Extinction training in conjunction with a partial agonist of the glycine site on the NMDA receptor erases memory trace. J Neurosci. 2006;26:8892-8899.
44. Falls WA, Miserendino MJ, Davis M. Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J. Neurosci. 1992;12:854-863.
45. Zimmwemn JM, Maren S. NMDA receptor antagonism in the basolateral but not central amygdale blocks the extinction of Pavlovian fear conditioning in rats. Eur J Neurosci. 2010;31:1664-1670.
46. Rocher C, Spedding M, Munoz C, Jay TM. Acute stress-induced changes in hippocampal prefrontal circuits in rats: effects of antidepressants. Cereb Cortex. 2004;14:224-229.
47. Li Z, Richter-Levin G. Stimulus intensity-dependent modulations of hippocampal ong-term potentiation by basolaeral amygdale priming. Front Cell Neurosci. 2012;6:1-9.
48. Ishikawa S, Saito Y, Yanagawa Y, Otani S, Hiraide S, Shimamura K, et al. Early postnatal stress alters extracellular signal-regulated kinase signaling in the corticolimbic system modulating emotional circuitry in adult rat. Eur J Neurosci. 2012;35:135-145.