Differential activation of amygdala, dorsal and ventral hippocampus following an exposure to a reminder of underwater trauma

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JAN, 2014, Pages

  Ritov, Gilad ^a   Ardi, Ziv ^a   Richter Levin, Gal ^a  

^a UNIVERSITY OF HAIFA   (Israel)

Author keywords

Amygdala; Emotional memory; PTSD; Rat model; Ventral hippocampus

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BEHAVIOR; CELL ACTIVATION; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DORSAL HIPPOCAMPUS; EMOTIONAL STRESS; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; NERVE CELL; NEUROPHYSIOLOGY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PSYCHOTRAUMA; RAT; UNDERWATER TRAUMA; VENTRAL HIPPOCAMPUS;

EID: 84893199052     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00018     Document Type: Article

References (44)

1. Adams, J. P., and Sweatt, J. D. (2002). Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu. Rev. Pharmacol. Toxicol. 42, 135-163. doi: 10.1146/annurev.pharmtox.42.082701.145401
2. American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders. 5th Edn. Washington: The Association.
3. Antoine, B., Laroche, S., and Caboche, J. (2013). Comparative dynamics of MAPK/ERK signalling components and immediate early genes in the hippocampus and amygdala following contextual fear conditioning and retrieval. Brain Struct. Funct. 219, 415-430. doi: 10.1007/s00429-013-0505-y
4. Ardi, Z., Ritov, G., Lucas, M., and Richter-Levin, G. (2013). The effects of a reminder of underwater trauma on behavior and memory-related mechanisms in the rat dentate gyrus. Int. J. Neuropsychopharmacol. doi: 10.1017/S1461145713001272. [Epub ahead of print].
5. Armony, J. L., and LeDoux, J. E. (1997). How the brain processes emotional information. Ann. N Y Acad. Sci. 821, 259-270. doi: 10.1111/j.1749-6632.1997.tb48285.x
6. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., and Sweatt, J. D. (1998). The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1, 602-609. doi: 10.1038/2836
7. Bergado, J. A., Lucas, M., and Richter-Levin, G. (2011). Emotional tagging-a simple hypothesis in a complex reality. Prog. Neurobiol. 94, 64-76. doi: 10.1016/j.pneurobio.2011.03.004
8. Cahill, L., and McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21, 294-299. doi: 10.1016/s0166-2236(97)01214-9
9. Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D., and Cahill, L. (2000). Event-related activation in the human amygdala associates with later memory for individual emotional experience. J. Neurosci. 20:RC99.
10. Caudal, D., Godsil, B. P., Mailliet, F., Bergerot, D., and Jay, T. M. (2010). Acute stress induces contrasting changes in ampa receptor subunit phosphorylation within the prefrontal cortex, amygdala and hippocampus. PLoS One 5:e15282. doi: 10.1371/journal.pone.0015282
11. Cohen, H., Kaplan, Z., Matar, M. A., Buriakovsky, I., Bourin, M., and Kotler, M. (2004). Different pathways mediated by CCK1 and CCK2 receptors: effect of intraperitonal mrna antisense oligodeoxynucleotides to cholecystokinin on anxiety-like and learning behaviors in rats. Depress. Anxiety 20, 139-152. doi: 10.1002/da.20032
12. Cohen-Matsliah, S. I., Brosh, I., Rosenblum, K., and Barkai, E. (2007). A novel role for extracellular signal-regulated kinase in maintaining long-term memory-relevant excitability changes. J. Neurosci. 27, 12584-12589. doi: 10.1523/jneurosci.3728-07.2007
13. Cryan, J. F., Valentino, R. J., and Lucki, I. (2005). Assessing substrats underlying the behavioral effects of antideprressants using the modified rat forced swimming test. Neurosci. Biobehav. Rev. 29, 547-569. doi: 10.1016/j.neubiorev.2005.03.008
14. Fanselow, M. S., and Dong, H.-W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19. doi: 10.1016/j.neuron.2009.11.031
15. Gilboa, A., Shalev, A. Y., Laor, L., Lester, H., Louzoun, Y., Chisin, R., et al. (2004). Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biol. Psychiatry 55, 263-272. doi: 10.1016/j.biopsych.2003.08.004
16. Goosens, K. A. (2011). Hippocampal regulation of aversive memories. Curr. Opin. Neurobiol.21, 460-466. doi: 10.1016/j.conb.2011.04.003
17. Howland, J. G., and Wang, Y. T. (2008). Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog. Brain Res. 169, 145-158. doi: 10.1016/s0079-6123(07)00008-8
18. Ilin, Y., and Richter-Levin, G. (2009). ERK2 and CREB activation in the amygdala when an event is remembered as "Fearful" and not when it is remembered as "Instructive". J. Neurosci. Res. 87, 1823-1831. doi: 10.1002/jnr.21994
19. Kogan, I., and Richter-Levin, G. (2008). Activation pattern of the limbic system following spatial learning under stress. Eur. J. Neurosci. 27, 715-722. doi: 10.1111/j.1460-9568.2008.06034.x
20. Korz, V., and Frey, J. U. (2003). Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors. J. Neurosci. 23, 7281-7287.
21. Lanius, R. A., Williamson, P. C., Densmore, M., Boksman, K., Neufeld, R. W., Gati, J. S., et al. (2004). The nature of traumatic memories: a 4-T FMRI functional connectivity analysis. Am. J. Psychiatry 161, 36-44. doi: 10.1176/appi.ajp.161.1.36
22. LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184. doi: 10.1146/annurev.neuro.23.1.155
23. LeDoux, J. (2003). The emotional brain, fear and the amygdala. Cell. Mol. Neurobiol. 23, 727-738. doi: 10.1023/A:1025048802629
24. Li, Z., and Richter-Levin, G. (2012). Stimulus intensity-dependent modulations of hippocampal long-term potentiation by basolateral amygdala priming. Front. Cell. Neurosci.6:21. doi: 10.3389/fncel.2012.00021
25. Liberzon, I., Taylor, S. F., Amdur, R., Jung, T. D., Chamberlain, K. R., Minoshima, S., et al. (1999). Brain activation in PTSD in response to trauma-related stimuli. Biol. Psychiatry 45, 817-826. doi: 10.1016/s0006-3223(98)00246-7
26. Maggio, N., and Segal, M. (2007). Unique regulation of long term potentiation in the rat ventral hippocampus. Hippocampus 17, 10-25. doi: 10.1002/hipo.20237
27. Maggio, N., and Segal, M. (2009). Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus. J. Neurosci. 29, 8633-8638. doi: 10.1523/jneurosci.1901-09.2009
28. McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1-28. doi: 10.1146/annurev.neuro.27.070203.144157
29. Paxinos, G., and Watson, C. (2005). The Rat Brain in Stereotaxic Coordinates. 5th Edn. San Diego: Academic Press.
30. Pitkanen, A., Pikkarainen, M., Nurminen, N., and Ylinen, A. (2000). Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex and postrhinal cortex in rat. A review. Ann. N Y Acad. Sci. 911, 369-391. doi: 10.1111/j.1749-6632.2000.tb06738.x
31. Richter-Levin, G. (1998). Acute and long-term behavioral correlates of underwater trauma-potential relevance to stress and post-stress syndromes. Psychiatry Res. 79, 73-83. doi: 10.1016/s0165-1781(98)00030-4
32. Richter-Levin, G. (2004). The amygdala, the hippocampus and emotional modulation of memory. Neuroscientist 10, 31-39. doi: 10.1177/1073858403259955
33. Richter-Levin, G., and Akirav, I. (2003). Emotional tagging of memory formation-in the search for neural mechanisms. Brain Res. Brain Res. Rev. 43, 247-256. doi: 10.1016/j.brainresrev.2003.08.005
34. Roozendaal, B., McEwen, B. S., and Chattarji, S. (2009). Stress, memory and the amygdala. Nat. Rev. Neurosci. 10, 423-433. doi: 10.1038/nrn2651
35. Satpute, A. B., Mumford, J. A., Naliboff, B. D., and Poldrack, R. A. (2012). Human anterior and posterior hippocampus respond distinctly to state and trait anxiety. Emotion 12, 58-68. doi: 10.1037/a0026517
36. Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., and Oitzl, M. S. (2012). Stress effects on memory: an update and integration. Neurosci. Biobehav. Rev. 36, 1740-1749. doi: 10.1016/j.neubiorev.2011.07.002
37. Segal, M., Richter-Levin, G., and Maggio, N. (2010). Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20, 1332-1338. doi: 10.1002/hipo.20751
38. Squire, L. R., and Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science253, 1380-1386. doi: 10.1126/science.1896849
39. Sweatt, J. D. (2001). The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76, 1-10. doi: 10.1046/j.1471-4159.2001.00054.x
40. Sweatt, J. D. (2004). Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 14, 311-317. doi: 10.1016/j.conb.2004.04.001
41. Tronel, S., and Alberini, C. M. (2007). Persistent disruption of a traumatic memory by postretrieval inactivation of glucocorticoid receptors in the amygdala. Biol. Psychiatry 62, 33-39. doi: 10.1016/j.biopsych.2006.09.009
42. Vouimba, R. M., and Richter-Levin, G. (2013). Different patterns of amygdala priming differentially affect dentate gyrus plasticity and corticosterone, but not CA1 plasticity. Front. Neural Circuits 7:80. doi: 10.3389/fncir.2013.00080
43. Wang, J., Akirav, I., and Richter-Levin, G. (2000). Short-term behavioral and electrophysiological consequences of underwater trauma. Physiol. Behav. 70, 327-332. doi: 10.1016/s0031-9384(00)00274-2
44. Zald, D. H. (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Res. Brain Res. Rev. 41, 88-123. doi: 10.1016/s0165-0173(02)00248-5