Molecular Neurobiology

, Volume 55, Issue 5, pp 4107–4114 | Cite as

Long-Term Plasticity in Amygdala Circuits: Implication of CB1-Dependent LTD in Stress

Article

Abstract

The amygdala mediates many forms of emotional learning, during which the central nucleus of amygdala (CeA) functions as a major output of the amygdala by converging inputs from the basolateral nucleus (BLA) and other amygdalar subregions. However, the contribution of BLA-CeA synaptic transmission and plasticity of this transmission after exposure to emotional stimuli remains to be completely understood. Using paired recording, we simultaneously recorded BLA and CeA neurons, and observed that BLA-CeA transmission was glutamatergic. In this transmission, high-frequency stimulation induced NMDA receptor (NMDAR)-dependent LTP, low-frequency stimulation induced NMDAR-dependent LTD, whereas modest-frequency stimulation induced cannabinoid receptor1 (CB1)-dependent LTD. After acute stress, CB1-dependent LTD of this transmission was selectively abolished. This effect of stress was mimicked by intra-CeA administration of CB1-selective agonists and prevented by CB1-selective antagonists. Furthermore, intra-CeA administration of CB1 antagonists prevented stress-induced reduction of explorative behaviors. These results indicate that CB1 signaling-mediated plasticity in local circuits of the amygdala plays a critical role in emotional responses.

Keywords

Amygdala Basolateral nucleus Central nucleus LTD CB1 

Notes

Acknowledgements

This work was supported by grants from the Natural Science Foundation of China (NSFC) (31571126, 31471120, 31540076, 31171123, 31300850) and Jilin Science and Technology Agency funding (20150307014YY).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Price JL, Drevets WC (2010) Neurocircuitry of mood disorders. Neuropsychopharmacology 35:192–216. doi: 10.1038/npp.2009.104 CrossRefPubMedGoogle Scholar
  2. 2.
    Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834. doi: 10.1152/physrev.00002.2003 CrossRefPubMedGoogle Scholar
  3. 3.
    Lutz B (2009) Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol 9:46–52. doi: 10.1016/j.coph.2008.12.001 CrossRefPubMedGoogle Scholar
  4. 4.
    Alger BE (2012) Endocannabinoids at the synapse a decade after the dies mirabilis (29 March 2001): what we still do not know. J Physiol 590:2203–2212. doi: 10.1113/jphysiol.2011.220855 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Rea K et al (2013) Evidence for a role of GABAergic and glutamatergic signalling in the basolateral amygdala in endocannabinoid-mediated fear-conditioned analgesia in rats. Pain 154:576–585. doi: 10.1016/j.pain.2012.12.021 CrossRefPubMedGoogle Scholar
  6. 6.
    McReynolds JR, McIntyre CK (2012) Emotional modulation of the synapse. Rev Neurosci 23:449–461. doi: 10.1515/revneuro-2012-0047 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391CrossRefPubMedGoogle Scholar
  8. 8.
    Glangetas C et al (2013) Stress switches cannabinoid type-1 (CB1) receptor-dependent plasticity from LTD to LTP in the bed nucleus of the stria terminalis. J Neurosci 33:19657–19663. doi: 10.1523/JNEUROSCI.3175-13.2013 CrossRefPubMedGoogle Scholar
  9. 9.
    Faraji J et al (2013) Stress inhibits psychomotor performance differently in simple and complex open field environments. Horm Behav 65:66–75. doi: 10.1016/j.yhbeh.2013.11.007 CrossRefPubMedGoogle Scholar
  10. 10.
    Huganir RL, Nicoll RA (2013) AMPARs and synaptic plasticity: The last 25 years. Neuron 80:704–717. doi: 10.1016/j.neuron.2013.10.025 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88. doi: 10.1126/science.1103944 CrossRefPubMedGoogle Scholar
  12. 12.
    Clem RL, Huganir RL (2013) Norepinephrine enhances a discrete form of long-term depression during fear memory storage. J Neurosci 33:11825–11832. doi: 10.1523/JNEUROSCI.3317-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Heifets BD, Castillo PE (2009) Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71:283–306. doi: 10.1146/annurev.physiol.010908.163149 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Akirav I (2013) Cannabinoids and glucocorticoids modulate emotional memory after stress. Neurosci Biobehav Rev 37:2554–2563. doi: 10.1016/j.neubiorev.2013.08.002 CrossRefPubMedGoogle Scholar
  15. 15.
    Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225–254. doi: 10.1002/cne.901780204 CrossRefPubMedGoogle Scholar
  16. 16.
    Ehrlich I et al (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771. doi: 10.1016/j.neuron.2009.05.026 CrossRefPubMedGoogle Scholar
  17. 17.
    Kim MJ et al (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223:403–410. doi: 10.1016/j.bbr.2011.04.025 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213–4225CrossRefPubMedGoogle Scholar
  19. 19.
    Hermann H, Lutz B (2005) Coexpression of the cannabinoid receptor type 1 with the corticotropin-releasing hormone receptor type 1 in distinct regions of the adult mouse forebrain. Neurosci Lett 375:13–18. doi: 10.1016/j.neulet.2004.10.080 CrossRefPubMedGoogle Scholar
  20. 20.
    Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535–550. doi: 10.1002/cne.903270406 CrossRefPubMedGoogle Scholar
  21. 21.
    Fourgeaud L et al (2004) A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J Neurosci 24:6939–6945. doi: 10.1523/JNEUROSCI.0671-04.2004 CrossRefPubMedGoogle Scholar
  22. 22.
    Mato S et al (2004) A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 7:585–586. doi: 10.1038/nn1251 CrossRefPubMedGoogle Scholar
  23. 23.
    Mathur BN, Lovinger DM (2012) Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front Pharmacol 3:66. doi: 10.3389/fphar.2012.00066 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14:609–625. doi: 10.1038/nrn3381 CrossRefPubMedGoogle Scholar
  25. 25.
    Kupferschmidt DA, Klas PG, Erb S (2012) Cannabinoid CB1 receptors mediate the effects of corticotropin-releasing factor on the reinstatement of cocaine seeking and expression of cocaine-induced behavioural sensitization. Br J Pharmacol 167:196–206. doi: 10.1111/j.1476-5381.2012.01983.x CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Jilin Provincial Key Laboratory on Molecular and Chemical GeneticSecond Hospital of Jilin UniversityChangchunPeople’s Republic of China

Personalised recommendations