Contextual Fear Extinction and Re-Extinction in Carioca High- and Low-Conditioned Freezing Rats
Author(s)
Vitor de Castro Gomes,
Laura Andrea León,
Daniel Mograbi,
Fernando Cardenas,
Jesus Landeira-Fernandez*
Affiliation(s)
Pontifícia Universidade Católica do Rio de Janeiro, Rio de Janeiro, Brasil. Universidade de S?o Paulo, Ribeir?o Preto, Brasil . Institute of Psychiatry, Kings College, London, UK. Universidad de los Andes, Bogotá, Col?mbia .
Pontifícia Universidade Católica do Rio de Janeiro, Rio de Janeiro, Brasil. Universidade de S?o Paulo, Ribeir?o Preto, Brasil . Institute of Psychiatry, Kings College, London, UK. Universidad de los Andes, Bogotá, Col?mbia .
ABSTRACT
We recently reported two novel breeding lines of rats known as Carioca High- and Low-conditioned Freezing (CHF and CLF), based on defensive freezing responses to contextual cues previously associated with electric footshock. The present study used animals of the 8th generation of our selective breeding program to investigate both contextual fear extinction and re-extinction. The results consistently showed that CHF animals froze more than CLF animals. Long extinction training was able to extinguish phenotypic differences between lines, but the divergence was restored after just one fear reacquisition training session. These differences disappeared again during re-extinction training. The possible neural mechanisms involved in these two types of learning are discussed.
Cite this paper
Gomes, V. , León, L. , Mograbi, D. , Cardenas, F. and Landeira-Fernandez, J. (2014) Contextual Fear Extinction and Re-Extinction in Carioca High- and Low-Conditioned Freezing Rats. World Journal of Neuroscience, 4, 247-252. doi: 10.4236/wjns.2014.43028.
Gomes, V. , León, L. , Mograbi, D. , Cardenas, F. and Landeira-Fernandez, J. (2014) Contextual Fear Extinction and Re-Extinction in Carioca High- and Low-Conditioned Freezing Rats. World Journal of Neuroscience, 4, 247-252. doi: 10.4236/wjns.2014.43028.
References
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http://dx.doi.org/10.1101/lm.1463909 [10] Quirk, G.J., Garcia, R. and González-Lima, F. (2006) Prefrontal Mechanisms in Extinction of Conditioned Fear. Biological Psychiatry, 60, 337-343.
http://dx.doi.org/10.1016/j.biopsych.2006.03.010 [11] Monfills, M.H., Cowansage, K.K., Klann, E. and Ledoux, J.E. (2009) Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories. Science, 324, 951-955.
http://dx.doi.org/10.1126/science.1167975 [12] Lattal, K.M., Radulovic, J. and Lukowiak, K. (2006) Extinction: [corrected] Does It or Doesn’t It? The Requirement of Altered Gene Activity and New Protein Synthesis. Biological Psychiatry, 60, 344-351.
http://dx.doi.org/10.1016/j.biopsych.2006.05.038 [13] Langton, J.M. and Richardson, R. (2009) The Role of Context in the Re-Extinction of Learned Fear. Neurobiology of Learning and Memory, 92, 496-503. http://dx.doi.org/10.1016/j.nlm.2009.06.008 [14] Langton, J.M. and Richardson, R. (2008) D-Cycloserine Facilitates Extinction the First Time but Not the Second Time: an Examination of the Role of NMDA across the Course of Repeated Extinction Sessions. Neuropsychopharmacology, 33, 3096-3102. http://dx.doi.org/10.1038/npp.2008.32 [15] Laurent, V., Marchand, A.R. and Westbrook, R.F. (2008) The Basolateral Amygdala Is Necessary for Learning but Not Relearning Extinction of Context Conditioned Fear. Learning and Memory, 15, 304-314.
http://dx.doi.org/10.1101/lm.928208 [16] Gomes, V.C. and Landeira-Fernandez, J. (2008). Amygdaloid Lesions Produced Similar Contextual Fear Conditioning Disruption in the Carioca Highand Low-Conditioned Freezing Rats. Brain Research, 1233, 137-145.
http://dx.doi.org/10.1016/j.brainres.2008.07.044 [17] Dias, G.P., et al. (2014) Hippocampal Biomarkers of Fear Memory in an Animal Model of Generalized Anxiety Disorder. Behavioural Brain Research, 263, 34-45.
http://dx.doi.org/10.1016/j.bbr.2014.01.012 [18] Galvao, B.O., Gomes, V.C., Maisonnette, S. and Landeira-Fernandez, J. (2011) Panic-Like Behaviors in Carioca High- and Low-Conditioned Freezing Rats. Psychology and Neuroscience, 4, 205-210.
http://dx.doi.org/10.3922/j.psns.2011.2.005 [19] Gomes, V.C., Silva, C.E.B. and Landeira-Fernandez, J. (2011) The Carioca High- and Low-Conditioned Freezing Lines: A New Animal Model of Generalized Anxiety Disorder. In: Kalinin, V., Ed., Anxiety Disorders, InTech, Rijeka, 121-134. http://dx.doi.org/10.5772/23598 [20] Hassan, W., Gomes, V.C., Pinton, S., Batista Teixeira da Rocha, J. and Landeira-Fernandez, J. (2013) Association between Oxidative Stress and Contextual Fear Conditioning in Carioca Highand Low-Conditioned Freezing Rats. Brain Research, 28, 60-67.
http://dx.doi.org/10.1016/j.brainres.2013.03.039 [21] Gale, G.D., et al. (2004) Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats. Journal of Neuroscience, 24, 3810-3815.
http://dx.doi.org/10.1523/JNEUROSCI.4100-03.2004 [22] Fanselow, M.S. and Gale, G.D. (2003) The Amygala, Fear, and Memory. Annals of the New York Academy of Sciences, 985, 125-134. http://dx.doi.org/10.1111/j.1749-6632.2003.tb07077.x [23] Leung, H.T., Bailey, G.K., Laurent, V. and Westbrook, R.F. (2007) Rapid Reacquisition of Fear to a Completely Extinguished Context is Replaced by Transient Impairment with Additional Extinction Training. Journal of Experimental Psychology: Animal Learning and Cognition, 33, 299-313. http://dx.doi.org/10.1037/0097-7403.33.3.299 [24] Motanis, H. and Maroun, M. (2012) Differential Involvement of Protein Synthesis and Actin Rearrangement in the Reacquisition of Contextual Fear Conditioning. Hippocampus, 22, 494-500. http://dx.doi.org/10.1002/hipo.20915 [25] Bergstrom, H.C., McDonald, C.G., Dey, S., Tang, H., Selwyn, R.G. and Johnson, L.R. (2013) The Structure of Pavlovian Fear Conditioning in the Amygdala. Brain Structure and Function, 218, 1569-1589.
http://dx.doi.org/10.1007/s00429-012-0478-2 [26] Chang, C.H. and Maren, S. (2011) Medial Prefrontal Cortex Activation Facilitates Re-Extinction of Fear in Rats. Learning and Memory, 18, 221-225. http://dx.doi.org/10.1101/lm.2070111
[1] Fanselow, M.S. (1984) What Is Conditioned Fear? Trends in Neurosciences, 7, 460-462.
http://dx.doi.org/10.1016/S0166-2236(84)80253-2 [2] Sigmundi, R.A., Bouton, M.E. and Bolles, R.C. (1980) Conditioned Freezing in the Rat as a Function of Shock Intensity and CS Modality. Bulletin of the Psychonomic Society, 15, 254-256. [3] Landeira-Fernandez, J. (1996) Context and Pavlovian Conditioning. Brazilian Journal of Medical and Biological Research, 29, 149-173. [4] Maren, S. (2011) Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory. Neuron, 70, 830-845. [5] Vervliet, B., Craske, M.G. and Hermans, D. (2013) Fear Extinction and Relapse: State of the Art. Annual Review of Clinical Psychology, 9, 215-248. http://dx.doi.org/10.1146/annurev-clinpsy-050212-185542 [6] Herry, C., Ferraguti, F., Singewald, N., Letzkus, J.J., Ehrlich, I. and Lüthi, A. (2010) Neuronal Circuits of Fear Extinction. European Journal of Neuroscience, 31, 599-612. http://dx.doi.org/10.1111/j.1460-9568.2010.07101.x [7] Ji, J. and Maren, S. (2007) Hippocampal Involvement in Contextual Modulation of Fear Extinction. Hippocampus, 17, 749-758. [8] Knapska, E., et al. (2012) Functional Anatomy of Neural Circuits Regulating Fear and Extinction. Proceedings of the National Academy of Sciences of the United States of America, 109, 17093-17098.
http://dx.doi.org/10.1073/pnas.1202087109 [9] Knapska, E. and Maren, S. (2009) Reciprocal Patterns of c-Fos Expression in the Medial Prefrontal Cortex and Amygdala After Extinction and Renewal of Conditioned Fear. Learning and Memory, 16, 486-493.
http://dx.doi.org/10.1101/lm.1463909 [10] Quirk, G.J., Garcia, R. and González-Lima, F. (2006) Prefrontal Mechanisms in Extinction of Conditioned Fear. Biological Psychiatry, 60, 337-343.
http://dx.doi.org/10.1016/j.biopsych.2006.03.010 [11] Monfills, M.H., Cowansage, K.K., Klann, E. and Ledoux, J.E. (2009) Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories. Science, 324, 951-955.
http://dx.doi.org/10.1126/science.1167975 [12] Lattal, K.M., Radulovic, J. and Lukowiak, K. (2006) Extinction: [corrected] Does It or Doesn’t It? The Requirement of Altered Gene Activity and New Protein Synthesis. Biological Psychiatry, 60, 344-351.
http://dx.doi.org/10.1016/j.biopsych.2006.05.038 [13] Langton, J.M. and Richardson, R. (2009) The Role of Context in the Re-Extinction of Learned Fear. Neurobiology of Learning and Memory, 92, 496-503. http://dx.doi.org/10.1016/j.nlm.2009.06.008 [14] Langton, J.M. and Richardson, R. (2008) D-Cycloserine Facilitates Extinction the First Time but Not the Second Time: an Examination of the Role of NMDA across the Course of Repeated Extinction Sessions. Neuropsychopharmacology, 33, 3096-3102. http://dx.doi.org/10.1038/npp.2008.32 [15] Laurent, V., Marchand, A.R. and Westbrook, R.F. (2008) The Basolateral Amygdala Is Necessary for Learning but Not Relearning Extinction of Context Conditioned Fear. Learning and Memory, 15, 304-314.
http://dx.doi.org/10.1101/lm.928208 [16] Gomes, V.C. and Landeira-Fernandez, J. (2008). Amygdaloid Lesions Produced Similar Contextual Fear Conditioning Disruption in the Carioca Highand Low-Conditioned Freezing Rats. Brain Research, 1233, 137-145.
http://dx.doi.org/10.1016/j.brainres.2008.07.044 [17] Dias, G.P., et al. (2014) Hippocampal Biomarkers of Fear Memory in an Animal Model of Generalized Anxiety Disorder. Behavioural Brain Research, 263, 34-45.
http://dx.doi.org/10.1016/j.bbr.2014.01.012 [18] Galvao, B.O., Gomes, V.C., Maisonnette, S. and Landeira-Fernandez, J. (2011) Panic-Like Behaviors in Carioca High- and Low-Conditioned Freezing Rats. Psychology and Neuroscience, 4, 205-210.
http://dx.doi.org/10.3922/j.psns.2011.2.005 [19] Gomes, V.C., Silva, C.E.B. and Landeira-Fernandez, J. (2011) The Carioca High- and Low-Conditioned Freezing Lines: A New Animal Model of Generalized Anxiety Disorder. In: Kalinin, V., Ed., Anxiety Disorders, InTech, Rijeka, 121-134. http://dx.doi.org/10.5772/23598 [20] Hassan, W., Gomes, V.C., Pinton, S., Batista Teixeira da Rocha, J. and Landeira-Fernandez, J. (2013) Association between Oxidative Stress and Contextual Fear Conditioning in Carioca Highand Low-Conditioned Freezing Rats. Brain Research, 28, 60-67.
http://dx.doi.org/10.1016/j.brainres.2013.03.039 [21] Gale, G.D., et al. (2004) Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats. Journal of Neuroscience, 24, 3810-3815.
http://dx.doi.org/10.1523/JNEUROSCI.4100-03.2004 [22] Fanselow, M.S. and Gale, G.D. (2003) The Amygala, Fear, and Memory. Annals of the New York Academy of Sciences, 985, 125-134. http://dx.doi.org/10.1111/j.1749-6632.2003.tb07077.x [23] Leung, H.T., Bailey, G.K., Laurent, V. and Westbrook, R.F. (2007) Rapid Reacquisition of Fear to a Completely Extinguished Context is Replaced by Transient Impairment with Additional Extinction Training. Journal of Experimental Psychology: Animal Learning and Cognition, 33, 299-313. http://dx.doi.org/10.1037/0097-7403.33.3.299 [24] Motanis, H. and Maroun, M. (2012) Differential Involvement of Protein Synthesis and Actin Rearrangement in the Reacquisition of Contextual Fear Conditioning. Hippocampus, 22, 494-500. http://dx.doi.org/10.1002/hipo.20915 [25] Bergstrom, H.C., McDonald, C.G., Dey, S., Tang, H., Selwyn, R.G. and Johnson, L.R. (2013) The Structure of Pavlovian Fear Conditioning in the Amygdala. Brain Structure and Function, 218, 1569-1589.
http://dx.doi.org/10.1007/s00429-012-0478-2 [26] Chang, C.H. and Maren, S. (2011) Medial Prefrontal Cortex Activation Facilitates Re-Extinction of Fear in Rats. Learning and Memory, 18, 221-225. http://dx.doi.org/10.1101/lm.2070111