Lateral Habenula determines long-term storage of aversive memories

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Tomaiuolo, Micol ^a   Gonzalez, Carolina ^a   Medina, Jorge H ^a,b   Piriz, Joaquin ^c,d  

^a Facultad de Medicina   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Buenos Aires   (Argentina)

^d INSTITUTO DE FISIOLOGÍA   (Argentina)

Author keywords

Fear memory; Inhibitory avoidance learning; Lateral Habenula; Memory persistence; Rats; Wistar

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; FEAR; HABENULA; LATERAL HABENULA; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NONHUMAN; OPEN FIELD TEST; PASSIVE AVOIDANCE TEST; RAT; STATE DEPENDENT LEARNING;

EID: 84901334271     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00170     Document Type: Article

References (37)

1. Aizawa, H., Yanagihara, S., Kobayashi, M., Niisato, K., Takekawa, T., Harukuni, R., et al. (2013). The synchronous activity of lateral habenular neurons is essential for regulating hippocampal theta oscillation. J. Neurosci. 33, 8909-8921. doi: 10.1523/JNEUROSCI.4369-12.2013
2. Alberini, C. M. (2008). The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol. Learn. Mem. 89, 234-246. doi: 10.1016/j.nlm.2007.08.007
3. Bekinschtein, P., Cammarota, M., Igaz, L. M., Bevilaqua, L. R., Izquierdo, I., and Medina, J. H. (2007). Persistence of long-term memory storage requires a late protein synthesis-and BDNF-dependent phase in the hippocampus. Neuron 53, 261-277. doi: 10.1016/j.neuron.2006.11.025
4. Christoph, G. R., Leonzio, R. J., and Wilcox, K. S. (1986). Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J. Neurosci. 6, 613-619.
5. Fadok, J. P., Dickerson, T. M., and Palmiter, R. D. (2009). Dopamine is necessary for cue-dependent fear conditioning. J. Neurosci. 29, 11089-11097. doi: 10.1523/JNEUROSCI.1616-09.2009
6. Friedman, A., Lax, E., Dikshtein, Y., Abraham, L., Flaumenhaft, Y., Sudai, E., et al. (2011). Electrical stimulation of the lateral habenula produces an inhibitory effect on sucrose self-administration. Neuropharmacology 60, 381-387. doi: 10.1016/j.neuropharm.2010.10.006
7. Gold, P. E. (1986). The use of avoidance training in studies of modulation of memory storage. Behav. Neural Biol. 46, 87-98.
8. Gold, P. E. (2008). Protein synthesis inhibition and memory: formation vs amnesia. Neurobiol. Learn. Mem. 89, 201-211. doi: 10.1016/j.nlm.2007.10.006
9. Goutagny, R., Loureiro, M., Jackson, J., Chaumont, J., Williams, S., Isope, P., et al. (2013). Interactions between the lateral habenula and the hippocampus: implication for spatial memory processes. Neuropsychopharmacology 38, 2418-2426. doi: 10.1038/npp.2013.142
10. Guzmán-Ramos, K., Osorio-Gómez, D., Moreno-Castilla, P., and Bermúdez-Rattoni, F. (2010). Off-line concomitant release of dopamine and glutamate involvement in taste memory consolidation. J. Neurochem. 114, 226-236. doi: 10.1111/j.1471-4159.2010.06758.x
11. Hikosaka, O. (2010). The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 11, 503-513. doi: 10.1038/nrn2866
12. Ilango, A., Shumake, J., Wetzel, W., Scheich, H., and Ohl, F. W. (2013). Electrical stimulation of lateral habenula during learning: frequency-dependent effects on acquisition but not retrieval of a two-way active avoidance response. PLoS ONE 8:e65684. doi: 10.1371/journal.pone.0065684
13. Izquierdo, I., and Medina, J. H. (1997). Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68, 285-316.
14. Ji, H., and Shepard, P. D. (2007). Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA(A) receptor-mediated mechanism. J. Neurosci. 27, 6923-6930. doi: 10.1523/JNEUROSCI.0958-07.2007
15. Katche, C., Bekinschtein, P., Slipczuk, L., Goldin, A., Izquierdo, I., Cammarota, M., et al. (2010). Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc. Natl. Acad. Sci. U.S.A. 107, 349-354. doi: 10.1073/pnas.0912931107
16. Katche, C., Dorman, G., Gonzalez, C., Kramar, C. P., Slipczuk, L., Rossato, J. I., et al. (2013). On the role of retrosplenial cortex in long-lasting memory storage. Hippocampus 23, 295-302. doi: 10.1002/hipo.22092
17. Kramar, C. P., Chefer, V. I., Wise, R. A., Medina, J. H., and Barbano, M. F. (2014). Dopamine in the dorsal hippocampus impairs the late consolidation of cocaine-associated memory. Neuropsychopharmacology 20. doi: 10.1038/npp.2014.11. [Epub ahead of print].
18. Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., et al. (2012). Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217. doi: 10.1038/nature11527
19. Lauzon, N. M., Ahmad, T., and Laviolette, S. R. (2012). Dopamine D4 receptor transmission in the prefrontal cortex controls the salience of emotional memory via modulation of calcium calmodulin-dependent kinase II. Cereb. Cortex 22, 2486-2494. doi: 10.1093/cercor/bhr326
20. Lecourtier, L., Neijt, H. C., and Kelly, P. H. (2004). Habenula lesions cause impaired cognitive performance in rats: implications for schizophrenia. Eur. J. Neurosci. 19, 2551-2560. doi: 10.1111/j.0953-816X.2004.03356.x
21. Matsumoto, M., and Hikosaka, O. (2007). Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447, 1111-1115. doi: 10.1038/nature05860
22. Moncada, D., and Viola, H. (2007). Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci. 27, 7476-7481. doi: 10.1523/JNEUROSCI.1083-07.2007
23. Ou, L. C., Yeh, S. H., and Gean, P. W. (2010). Late expression of brain-derived neurotrophic factor in the amygdala is required for persistence of fear memory. Neurobiol. Learn. Mem. 93, 372-382. doi: 10.1016/j.nlm.2009.12.003
24. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates, 6th Edn. Amsterdam; Oxford: Elsevier Academic.
25. Rossato, J. I., Bevilaqua, L. R. M., Izquierdo, I., Medina, J. H., and Cammarota, M. (2009). Dopamine controls persistence of long-term memory storage. Science 325, 1017-1020. doi: 10.1126/science.1172545
26. Schultz, W. (2007). Behavioral dopamine signals. Trends Neurosci. 30, 203-210. doi: 10.1016/j.tins.2007.03.007
27. Shabel, S. J., Proulx, C. D., Trias, A., Murphy, R. T., and Malinow, R. (2012). Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74, 475-481. doi: 10.1016/j.neuron.2012.02.037
28. Shumake, J., Ilango, A., Scheich, H., Wetzel, W., and Ohl, F. W. (2010). Differential neuromodulation of acquisition and retrieval of avoidance learning by the lateral habenula and ventral tegmental area. J. Neurosci. 30, 5876-5883. doi: 10.1523/JNEUROSCI.3604-09.2010
29. 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
30. Stopper, C. M., and Floresco, S. B. (2014). What's better for me? Fundamental role for lateral habenula in promoting subjective decision biases. Nat. Neurosci. 17, 33-35. doi: 10.1038/nn.3587
31. Thornton, E. W., and Bradbury, G. E. (1989). Effort and stress influence the effect of lesion of the habenula complex in one-way active avoidance learning. Physiol. Behav. 45, 929-935.
32. Tsai, H. C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., et al. (2009). Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084. doi: 10.1126/science.1168878
33. Vale-Martínez, A., Martí-Nicolovius, M., Guillazo-Blanch, G., Coll-Andreu, M., and Morgado-Bernal, I. (1997). Effects of habenular lesions upon two-way active avoidance conditioning in rats. Neurobiol. Learn. Mem. 68, 68-74.
34. Wang, D. G., Gong, N., Luo, B., and Xu, T. L. (2006). Absence of GABA type A signaling in adult medial habenular neurons. Neuroscience 141, 133-141. doi: 10.1016/j.neuroscience.2006.03.045
35. Wilcox, K. S., Christoph, G. R., Double, B. A., and Leonzio, R. J. (1986). Kainate and electrolytic lesions of the lateral habenula: effect on avoidance responses. Physiol. Behav. 36, 413-417.
36. Yang, C., Liu, J. F., Chai, B. S., Fang, Q., Chai, N., Zhao, L. Y., et al. (2013). Stress within a restricted time window selectively affects the persistence of long-term memory. PLoS ONE 8:e59075. doi: 10.1371/journal.pone.0059075
37. Zweifel, L. S., Parker, J. G., Lobb, C. J., Rainwater, A., Wall, V. Z., Fadok, J. P., et al. (2009). Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. U.S.A. 106, 7281-7288. doi: 10.1073/pnas.0813415106