Inhibition of projections from the basolateral amygdala to the entorhinal cortex disrupts the acquisition of contextual fear

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Sparta, Dennis R ^a   Smithuis, Jim ^a   Stamatakis, Alice M ^a,b   Jennings, Joshua H ^a,b   Kantak, Pranish A ^a   Ung, Randall L ^a,b   Stuber, Garret D ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Amygdala; Channelrhodopsin 2; Fear conditioning; Glutamate; Halorhodopsin; Hippocampus; Optogenetics

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN ELECTROPHYSIOLOGY; COGNITION; CONDITIONING; CONTROLLED STUDY; ENTORHINAL CORTEX; EXPERIMENTAL SOCIAL BEHAVIOR TEST; FEAR; GLUTAMATERGIC PATHWAY; GLUTAMATERGIC PROJECTION; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOUSE; NERVE CELL INHIBITION; NERVE PROJECTION; NEUROTRANSMISSION; NONHUMAN;

EID: 84899840845     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00129     Document Type: Article

References (43)

1. Anagnostaras, S. G., Maren, S., and Fanselow, M. S. (1999). Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci. 19, 1106-1114.
2. Blanchard, D. C., and Blanchard, R. J. (1972). Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 81, 281-290. doi: 10.1037/h0033521
3. Blanchard, R. J., and Blanchard, D. C. (1969). Crouching as an index of fear. J. Comp. Physiol. Psychol. 67, 370-375. doi: 10.1037/h0026779
4. Bouton, M. E. (2002). Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol. Psychiatry 52, 976-986. doi: 10.1016/s0006-3223(02)01546-9
5. Bouton, M. E., and King, D. A. (1983). Contextual control of the extinction of conditioned fear: tests for the associative value of the context. J. Exp. Psychol. Anim. Behav. Process. 9, 248-265. doi: 10.1037/0097-7403.9.3.248
6. Davis, M. (1992). The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15, 353-375. doi: 10.1146/annurev.neuro.15.1.353
7. Davis, M. (1997). Neurobiology of fear responses: the role of the amygdala. J. Neuropsychiatry Clin. Neurosci. 9, 382-402.
8. de Vries, G. J., and Olff, M. (2009). The lifetime prevalence of traumatic events and posttraumatic stress disorder in the Netherlands. J. Trauma. Stress 22, 259-267. doi: 10.1002/jts.20429
9. Fanselow, M. S. (1980). Conditioned and unconditional components of post-shock freezing. Pavlov. J. Biol. Sci. 15, 177-182.
10. Felix-Ortiz, A. C., and Tye, K. M. (2014). Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J. Neurosci. 34, 586-595. doi: 10.1523/jneurosci.4257-13.2014
11. Felix-Ortiz, A. C., Beyeler, A., Seo, C., Leppla, C. A., Wildes, C. P., and Tye, K. M. (2013). BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 79, 658-664. doi: 10.1016/j.neuron.2013.06.016
12. Gentile, C. G., Jarrell, T. W., Teich, A., McCabe, P. M., and Schneiderman, N. (1986). The role of amygdaloid central nucleus in the retention of differential pavlovian conditioning of bradycardia in rabbits. Behav. Brain Res. 20, 263-273. doi: 10.1016/0166-4328(86)90226-3
13. Goosens, K. A., and Maren, S. (2001). Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem. 8, 148-155. doi: 10.1101/lm.37601
14. Goosens, K. A., and Maren, S. (2003). Pretraining NMDA receptor blockade in the basolateral complex, but not the central nucleus, of the amygdala prevents savings of conditional fear. Behav. Neurosci. 117, 738-750. doi: 10.1037/0735-7044.117.4.738
15. Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., et al. (2010). Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165. doi: 10.1016/j.cell.2010.02.037
16. Hall, J., Thomas, K. L., and Everitt, B. J. (2001). Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J. Neurosci. 21, 2186-2193.
17. Harris, J. A., Jones, M. L., Bailey, G. K., and Westbrook, R. F. (2000). Contextual control over conditioned responding in an extinction paradigm. J. Exp. Psychol. Anim. Behav. Process. 26, 174-185. doi: 10.1037/0097-7403.26.2.174
18. Herry, C., Ciocchi, S., Senn, V., Demmou, L., Muller, C., and Luthi, A. (2008). Switching on and off fear by distinct neuronal circuits. Nature 454, 600-606. doi: 10.1038/nature07166
19. Hitchcock, J., and Davis, M. (1986). Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav. Neurosci. 100, 11-22. doi: 10.1037/0735-7044.100.1.11
20. Jennings, J. H., Sparta, D. R., Stamatakis, A. M., Ung, R. L., Pleil, K. E., Kash, T. L., et al. (2013). Distinct extended amygdala circuits for divergent motivational states. Nature 496, 224-228. doi: 10.1038/nature12041
21. Ji, J., and Maren, S. (2008). Lesions of the entorhinal cortex or fornix disrupt the context-dependence of fear extinction in rats. Behav. Brain Res. 194, 201-206. doi: 10.1016/j.bbr.2008.07.011
22. Kapp, B. S., Frysinger, R. C., Gallagher, M., and Haselton, J. R. (1979). Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol. Behav. 23, 1109-1117. doi: 10.1016/0031-9384(79)90304-4
23. Kim, J. J., Rison, R. A., and Fanselow, M. S. (1993). Effects of amygdala, hippocampus, and periaqueductal gray lesions on short-and long-term contextual fear. Behav. Neurosci. 107, 1093-1098. doi: 10.1037//0735-7044.107.6.1093
24. Knapska, E., Macias, M., Mikosz, M., Nowak, A., Owczarek, D., Wawrzyniak, M., et al. (2012). Functional anatomy of neural circuits regulating fear and extinction. Proc. Natl. Acad. Sci. U S A 109, 17093-17098. doi: 10.1073/pnas.1202087109
25. Koch, S. B., van Zuiden, M., Nawijn, L., Frijling, J. L., Veltman, D. J., and Olff, M. (2014). Intranasal oxytocin as strategy for medication-enhanced psychotherapy of PTSD: salience processing and fear inhibition processes. Psychoneuroendocrinology 40C, 242-256. doi: 10.1016/j.psyneuen.2013.11.018
26. Lavond, D. G., Kim, J. J., and Thompson, R. F. (1993). Mammalian brain substrates of aversive classical conditioning. Annu. Rev. Psychol. 44, 317-342. doi: 10.1146/annurev.psych.44.1.317
27. Liberzon, I., and Sripada, C. S. (2008). The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res.167, 151-169. doi: 10.1016/s0079-6123(07)67011-3
28. Majchrzak, M., Ferry, B., Marchand, A. R., Herbeaux, K., Seillier, A., and Barbelivien, A. (2006). Entorhinal cortex lesions disrupt fear conditioning to background context but spare fear conditioning to a tone in the rat. Hippocampus 16, 114-124. doi: 10.1002/hipo.20138
29. Maren, S., and Fanselow, M. S. (1997). Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol. Learn. Mem. 67, 142-149. doi: 10.1006/nlme.1996.3752
30. Maren, S., and Hobin, J. A. (2007). Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala. Learn. Mem. 14, 318-324. doi: 10.1101/lm.477007
31. Maren, S., Phan, K. L., and Liberzon, I. (2013). The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14, 417-428. doi: 10.1038/nrn3492
32. Nadel, L. (1987). A brain structure: the hippocampus. Science 235:1682a. doi: 10.1126/science.1682a
33. Orsini, C. A., Kim, J. H., Knapska, E., and Maren, S. (2011). Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. J. Neurosci. 31, 17269-17277. doi: 10.1523/jneurosci.4095-11.2011
34. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285. doi: 10.1037//0735-7044.106.2.274
35. Pitkänen, 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
36. Rougemont-Bucking, A., Linnman, C., Zeffiro, T. A., Zeidan, M. A., Lebron-Milad, K., Rodriguez-Romaguera, J., et al. (2011). Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci. Ther. 17, 227-236. doi: 10.1111/j.1755-5949.2010.00152.x
37. Sparta, D. R., Stamatakis, A. M., Phillips, J. L., Hovelso, N., van Zessen, R., and Stuber, G. D. (2011). Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 7, 12-23. doi: 10.1038/nprot.2011.413
38. Stamatakis, A. M., and Stuber, G. D. (2012). Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat. Neurosci. 15, 1105-1107. doi: 10.1038/nn.3145
39. Ueki, A., Miwa, C., and Miyoshi, K. (1994). Impairment in the acquisition of passive and active avoidance learning tasks due to bilateral entorhinal cortex lesions. J. Neurol. Sci. 125, 14-21. doi: 10.1016/0022-510x(94)90236-4
40. van Zessen, R., Phillips, J. L., Budygin, E. A., and Stuber, G. D. (2012). Activation of VTA GABA neurons disrupts reward consumption. Neuron 73, 1184-1194. doi: 10.1016/j.neuron.2012.02.016
41. Winocur, G., and Olds, J. (1978). Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. J. Comp. Physiol. Psychol. 92, 312-321. doi: 10.1037/h0077468
42. Zimmerman, J. M., and Maren, S. (2010). NMDA receptor antagonism in the basolateral but not central amygdala blocks the extinction of Pavlovian fear conditioning in rats. Eur. J. Neurosci. 31, 1664-1670. doi: 10.1111/j.1460-9568.2010.07223.x
43. Zovkic, I. B., and Sweatt, J. D. (2013). Epigenetic mechanisms in learned fear: implications for PTSD. Neuropsychopharmacology 38, 77-93. doi: 10.1038/npp.2012.79