Please wait a minute...
Advances in Psychological Science    2019, Vol. 27 Issue (8) : 1417-1426     DOI: 10.3724/SP.J.1042.2019.01417
Regular Articles |
Modulating maladaptive human memory: Evidence from reconsolidation
LIU Peng1,2,SHEN Hongkui3
1 Department of Psychology, Institute of Education Sciences, Shanxi Normal University, Linfen 041000, China
2 Institute of Education, Modern College of Humanities and Sciences of Shanxi Normal University, Linfen 041000, China
3 Shanxi Normal University Network Information Center, Linfen 041000, China
Download: PDF(656 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks     Supporting Info

Stable memories may re-enter an unstable state when they are retrieved. Upon retrieval, a consolidated memory can be updated, strengthened, weakened, or even erased. This process is known as reconsolidation. Thus, reconsolidation interventions provide an opportunity to modify seemingly stable memories. Studies on the reconsolidation of maladaptive human memory emphasize the role of propranolol and behavioral intervention therapies in fear and episodic memory reconsolidation. Multiple cortical brain regions and neural circuits are involved in the reconsolidation of human fear and episodic memory. These include the amygdala, hippocampus, ventromedial prefrontal cortex (vmPFC), prefrontal cortex (PFC), the amygdale-vmPFC network, and the hippocampus-PFC network. Existing memories can be modified during reconsolidation by various interventions, such as drug treatment, behavioral therapy, or noninvasive brain stimulation. This introduces the possibility of using these strategies to treat memory disorders. However, there is a significant gap between the relevant basic research and the clinical application due to the complexity of pathologic memory formation. Therefore, additional experimental paradigms that more closely resemble clinical situations are required. Furthermore, the precise boundary conditions for reconsolidation disruption should be elucidated in a future study, as this will promote the clinical application of laboratory research.

Keywords maladaptive human memory      reconsolidation      clinical intervention      boundary conditions.     
ZTFLH:  B842  
Issue Date: 25 June 2019
E-mail this article
E-mail Alert
Articles by authors
Peng LIU
Hongkui SHEN
Cite this article:   
Peng LIU,Hongkui SHEN. Modulating maladaptive human memory: Evidence from reconsolidation[J]. Advances in Psychological Science, 2019, 27(8): 1417-1426.
URL:     OR
[1] 胡静初, 张蔚欣, 陈小婷, 王文清, 王子洁, 庄楚群, …郑希付 . (2019). 远期恐惧记忆再巩固更新机制的线索选择性特点. 心理学报, 51( 3), 316-323.
url: 研究点分析
[2] 曹杨婧文, 李俊娇, 陈伟, 杨勇, 胡琰健, 郑希付 . (2019). 条件性恐惧记忆消退的提取干预范式及其作用的神经机制. 心理科学进展, 27( 2), 268-277.
url: 研究点分析
[3] Akagi K., Yamada M., Saitoh A., Oka J. I., & Yamada M . (2018). Post-reexposure administration of riluzole attenuates the reconsolidation of conditioned fear memory in rats. Neuropharmacology, 131, 1-10.
[4] Alberini C.., &Ledoux J.E . (2013). Memory reconsolidation. Current Biology, 23( 17), 746-750.
[5] Alfei J. M., Monti R. I. F., Molina V. A., Bueno A. M., & Urcelay G. P . (2015). Prediction error and trace dominance determine the fate of fear memories after post-training manipulations. Learning & Memory, 22( 8), 385-400.
[6] Agren T., Engman J., Frick A., Bj?rkstrand J., Larsson E. M., Furmark T., & Fredrikson M . (2012). Disruption of reconsolidation erases a fear memory trace in the human amygdala. Science, 337( 6101), 1550-1552.
[7] Beckers T. &Kindt M., (2017). Memory reconsolidation interference as an emerging treatment for emotional disorders: Strengths, limitations, challenges, and opportunities. Annual Review of Clinical Psychology, 13, 99-121.
[8] Bj?rkstrand J., Agren T., ?hs F., Frick A., Larsson E. M., Hjorth O., … Fredrikson M . (2016). Disrupting reconsolidation attenuates long-term fear memory in the human amygdala and facilitates approach behavior. Current Biology, 26( 19), 2690-2695.
[9] Bj?rkstrand J., Agren T., Frick A., Engman J., Larsson E. M., Furmark T., & Fredrikson M . (2015). Disruption of memory reconsolidation erases a fear memory trace in the human amygdala: An 18-month follow-up. Plos One, 10( 7), e0129393.
[10] Blumberger D. M., Maller J. J., Thomson L., Mulsant B. H., Rajji T. K., Maher M., … Daskalakis Z. J . (2016). Unilateral and bilateral MRI-targeted repetitive transcranial magnetic stimulation for treatment-resistant depression: A randomized controlled study. Journal of Psychiatry Neuroscience, 41( 4), E58-66.
[11] Boccia M. M., Blake M. G., Acosta G. B., & Baratti C. M . (2006). Post-retrieval effects of icv infusions of hemicholinium in mice are dependent on the age of the original memory. Learning & Memory, 13( 3), 376-381.
[12] Brunet A., Orr S. P., Tremblay J., Robertson K., Nader K., & Pitman R. K . (2008). Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. Journal of Psychiatric Research, 42( 6), 503-506.
[13] Censor N., Dayan E., & Cohen L. G . (2014). Cortico- subcortical neuronal circuitry associated with reconsolidation of human procedural memories. Cortex, 58, 281-288.
[14] Censor N., Horovitz S. G., & Cohen L. G . (2014). Interference with existing memories alters offline intrinsic functional brain connectivity. Neuron, 81( 1), 69-76.
[15] ChanJ. C., &LaPaglia J.A . (2013). Impairing existing declarative memory in humans by disrupting reconsolidation. Proceedings of the National Academy of Sciences of the United States of America, 110( 23), 9309-9313.
[16] Chan W. Y. M., Leung H. T., Westbrook R. F., & McNally G. P . (2010). Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioning. Learning & Memory, 17( 10), 512-521.
[17] Coles M.., &Heimberg R.G . (2002). Memory biases in the anxiety disorders: Current status. Clinical Psychology Review, 22( 4), 587-627.
[18] Corinna B., Paola B., Giorgio C., & Marco D . (2018). Transcranial magnetic stimulation for the treatment of cocaine addiction: Evidence to date. Substance Abuse and Rehabilitation, 9, 11-21.
[19] Dayan E., Censor N., Buch E. R., Sandrini M., & Cohen L. G . (2013). Noninvasive brain stimulation: From physiology to network dynamics and back. Nature Neuroscience, 16( 7), 838-844.
[20] Davidson R.., &Irwin W., (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Sciences, 3( 1), 11-21.
[21] Diaz-Mataix L., Ruiz Martinez R. C., Schafe G. E., LeDoux J.E., & Doyere V . (2013). Detection of a temporal error triggers reconsolidation of amygdala-dependent memories. Current Biology, 23( 6), 467-472.
[22] Dinur-Klein L., Dannon P., Hadar A., Rosenberg O., Roth Y., Kotler M., & Zangen A . (2014). Smoking cessation induced by deep repetitive transcranial magnetic stimulation of the prefrontal and insular cortices: A prospective, randomized controlled trial. Biological Psychiatry, 76( 9), 742-749.
[23] Downar J., Blumberger D. M., & Daskalakis Z. J . (2016). Repetitive transcranial magnetic stimulation: An emerging treatment for medication-resistant depression. Canadian Medical Association Journal, 188( 16), 1175-1177.
[24] Drexler S. M., Merz C. J., Hamacher-Dang T. C., Tegenthoff M., & Wolf O. T . (2015). Effects of cortisol on reconsolidation of reactivated fear memories. Neuropsychopharmacology, 40( 13), 3036-3043.
[25] Elsey J. W.., &Kindt M., (2017). Tackling maladaptive memories through reconsolidation: From neural to clinical science. Neurobiology of Learning and Memory, 142( Pt A), 108-117.
[26] Feng P., Zheng Y., & Feng T. Y . (2015). Spontaneous brain activity following fear reminder of fear conditioning by using resting-state functional MRI. Scientific Reports, 5, 16701.
[27] Flavell C.., &Lee J. L.C . (2013). Reconsolidation and extinction of an appetitive Pavlovian memory. Neurobiology of Learning and Memory, 104, 25-31.
[28] Gazendam F. J., Kamphuis J. H., & Kindt M . (2013). Deficient safety learning characterizes high trait anxious individuals. Biological Psychology, 92( 2), 342-352.
[29] Gazendam F. J., Kamphuis J. H., Eigenhuis A., Huizenga H. M. H., Soeter M., Bos M. G. N., … Kindt M . (2015). Personality predicts individual variation in fear learning: A multilevel growth modeling approach. Clinical Psychological Science, 3( 2), 175-188.
[30] Golkar A., Bellander M., Olsson A., & ?hman A . (2012). Are fear memories erasable?-reconsolidation of learned fear with fear-relevant and fear-irrelevant stimuli. Frontiers in Behaviour Neuroscience, 6( 80).
[31] Herrold A. A., Kletzel S. L., Harton B. C., Chambers R. A., Jordan N., & Pape T. L . (2014). Transcranial magnetic stimulation: Potential treatment for co-occurring alcohol, traumatic brain injury and posttraumatic stress disorders. Neural Regeneration Research, 9( 19), 1712-1730.
[32] Hone-Blanchet A., Wensing T., & Fecteau S . (2014). The use of virtual reality in craving assessment and cue-exposure therapy in substance use disorders. Frontiers in Human Neuroscience, 8( 1), 844.
[33] Hupbach A., Hardt O., Gomez R., & Nadel L . (2008) The dynamics of memory: Context-dependent updating. Learning & Memory, 15( 8), 574-579.
[34] Inda M. C., Muravieva E. V., & Alberini C. M . (2011). Memory retrieval and the passage of time: From reconsolidation and strengthening to extinction. The Journal of Neuroscience, 31( 5), 1635-1643.
[35] Isserles M., Shalev A. Y., Roth Y., Peri T., Kutz I., Zlotnick E., & Zangen A . (2013). Effectiveness of deep transcranial magnetic stimulation combined with a brief exposure procedure in post-traumatic stress disorder-a pilot study. Brain Stimulation, 6( 3), 377-383.
[36] Kindt M. &Soeter M., (2013). Reconsolidation in a human fear conditioning study: A test of extinction as updating mechanism. Biological Psychology, 92( 1), 43-50.
[37] Kindt M. &Soeter M., (2018). Pharmacologically induced amnesia for learned fear is time and sleep dependent. Nature Communication, 9( 1), 1316.
[38] Kindt M., Soeter M., & Vervliet B . (2009). Beyond extinction: Erasing human fear responses and preventing the return of fear. Nature Neuroscience, 12( 3), 256-258.
[39] Kroes M. C. W., Tendolkar I., van Wingen G. A., van Waarde J. A., Strange B. A., & Fernandez G . (2014). An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans. Nature Neuroscience, 17( 2), 204-206.
[40] Kwapis J. L., Jarome T. J., Ferrara N. C., & Helmstetter F. J . (2017). Updating procedures can reorganize the neural circuit supporting a fear memory. Neuropsychopharmacology, 42( 8), 1688-1697.
[41] Kwapis J. L., Jarome T. J., & Helmstetter F. J . (2015). The role of the medial prefrontal cortex in trace fear extinction. Learning & Memory, 22( 1), 39-46.
[42] Lee J. L. C., Nader K., & Schiller D . (2017). An update on memory reconsolidation updating. Trends in Cognitive Sciences, 21( 7), 531-545.
[43] Maples-Keller J. L., Price M., Jovanovic T., Norrholm S. D., Odenat L., Post L., … Rothbaum B. O . (2017). Targeting memory reconsolidation to prevent the return of fear in patients with fear of flying. Depress Anxiety, 34( 7), 610-620.
[44] McGaugh J. . (2000). Memory-a century of consolidation. Science, 287( 5451), 248-251.
[45] McGaugh J. . (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27, 1-28.
[46] McGhee L. L., Maani C. V., Garza T. H., Desocio P. A., Gaylord K. M., & Black I. H . (2009). The effect of propranolol on posttraumatic stress disorder in burned service members. Journal of Burn Care & Research, 30( 1), 92-97.
[47] Merlo E., Milton A. L., & Everitt B.J . (2018). A novel retrieval-dependent memory process revealed by the arrest of ERK1/2 activation in the basolateral amygdala. Journal of Neuroscience, 38( 13), 3199-3207.
[48] Michael C.., &Diana M., (2016). Brain stimulation in addiction. Neuropsychopharmacology, 41( 12), 2798-2809.
[49] Miniussi C., Harris J. A., & Ruzzoli M . (2013). Modelling non-invasive brain stimulation in cognitive neuroscience. Neuroscience & Biobehavioral Reviews, 37( 8), 1702-1712.
[50] Mungee A., Kazzer P., Feeser M., Nitsche M. A., Schiller D., & Bajbouj M . (2014). Transcranial direct current stimulation of the prefrontal cortex: A means to modulate fear memories. Neuroreport, 25( 7), 480-484.
[51] Nader K. (2015). Reconsolidation and the dynamic nature of memory. Cold Spring Harbor Perspectives in Biology, 7( 10), a021782.
[52] Nader K., Schafe G. E., Le Doux J. E . (2000). Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature, 406( 6797), 722-726.
[53] Oyarzún J. P., Lopez-Barroso D., Fuentemilla L., Cucurell D., Pedraza C., Rodriguez-Fornells A., &de Diego- Balaguer R., .(2012). Updating fearful memories with extinction training during reconsolidation: A human study using auditory aversive stimuli. PLoS One, 7(6), e38849.
[54] Pi?eyro M. E., Monti R. I. F., Alfei J. M., Bueno A. M., & Urcelay G. P . (2014). Memory destabilization is critical for the success of the reactivation-extinction procedure. Learning & Memory, 21( 1), 46-54.
[55] Pitman R. . (1989). Post-traumatic stress disorder, hormones, and memory. Biological Psychiatry, 26( 3), 221-223.
[56] Pitman R. K., Sanders K. M., Zusman R. M., Healy A. R., Cheema F., Lasko N. B., … Orr S. P . (2002). Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biological Psychiatry, 51( 2), 189-192.
[57] Power A. E., Berlau D. J., McGaugh J. L., & Steward O . (2006). Anisomycin infused into the hippocampus fails to block “reconsolidation” but impairs extinction: The role of re-exposure duration. Learning & Memory, 13( 1), 27-34.
[58] Preston A.., &Eichenbaum H., (2013). Interplay of hippocampus and prefrontal cortex in memory. Current Biology, 23( 17), 764-773.
[59] Reznikov R. &Hamani C., (2017). Posttraumatic Stress Disorder: Perspectives for the Use of Deep Brain Stimulation. Neuromodulation, 20( 1), 7-14.
[60] Robinson M. J.., &Franklin K. B.J . (2010). Reconsolidation of a morphine place preference: Impact of the strength and age of memory on disruption by propranolol and midazolam. Behavioural Brain Research, 213( 2), 201-207.
[61] Rosenbaum S., Vancampfort D., Steel Z., Newby J., Ward P. B., & Stubbs B . (2015). Physical activity in the treatment of Post-traumatic stress disorder: A systematic review and meta-analysis. Psychiatry Research, 230( 2), 130-136.
[62] Sandrini M., Censor N., Mishoe J., & Cohen L. G . (2013). Causal role of prefrontal cortex in strengthening of episodic memories through reconsolidation. Current Biology, 23( 21), 2181-2184.
[63] Schiller D., Kanen J. W., LeDoux J. E., Monfils M. H., & Phelps E. A . (2013). Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proceedings of the National Academy of Sciences of the United States of America, 110( 50), 20040-20045.
[64] Schiller D., Monfils M. H., Raio C. M., Johnson D. C., Ledoux J. E., & Phelps E. A . (2010). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature, 463( 7277), 49-53.
[65] Schwabe L., Nader K., Wolf O. T., Beaudry T., & Pruessner J. C . (2012). Neural signature of reconsolidation impairments by propranolol in humans. Biological Psychiatry, 71( 4), 380-386.
[66] Schwabe L., Nader K., & Pruessner J. C . (2013). β-Adrenergic blockade during reactivation reduces the subjective feeling of remembering associated with emotional episodic memories. Biological Psychology, 92( 2), 227-232.
[67] Sevenster D., Beckers T., & Kindt M . (2012). Retrieval per se is not sufficient to trigger reconsolidation of human fear memory. Neurobiology of Learning and Memory, 97( 3), 338-345.
[68] Sevenster D., Beckers T., & Kindt M . (2013). Prediction error governs pharmacologically induced amnesia for learned fear. Science, 339( 6121), 830-833.
[69] Sevenster D., Beckers T., & Kindt M . (2014). Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning. Learning & Memory, 21( 11), 580-584.
[70] Shafi M. M., Westover M. B., Fox M. D., & Pascual-Leone A . (2012). Exploration and modulation of brain network interactions with noninvasive brain stimulation in combination with neuroimaging. European Journal of Neuroscience, 35( 6), 805-825.
[71] Shehata M., Abdou K., Choko K., Matsuo M., Nishizono H., & Inokuchi K . (2018). Autophagy enhances memory erasure through synaptic destabilization. Journal of Neuroscience, 38( 15), 3809-3822.
[72] Shiban Y., Brütting J., Pauli P., & Muhlberger A . (2015). Fear reactivation prior to exposure therapy: Does it facilitate the effects of VR exposure in a randomized clinical sample? Journal of Behavior Therapy and Experimental Psychiatry, 46, 133-140.
[73] Soeter M. &Kindt M., (2010). Dissociating response systems: Erasing fear from memory. Neurobiology of Learning and Memory, 94( 1), 30-41.
[74] Soeter M. &Kindt M., (2011). Disrupting reconsolidation: Pharmacological and behavioral manipulations. Learning & Memory, 18( 6), 357-366.
[75] Soeter M. &Kindt M., (2012 a). Erasing fear for an imagined threat event. Psychoneuroendocrinology, 37( 11), 1769-1779.
[76] Soeter M. &Kindt M., (2012 b). Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology, 37( 5), 1204-1215.
[77] Soeter M. &Kindt M., (2013). High trait anxiety: A challenge for disrupting fear memory reconsolidation. Plos One, 8( 11), e75239.
[78] Soeter M. &Kindt M., (2015). An abrupt transformation of phobic behavior after a post-retrieval amnesic agent. Biological Psychiatry, 78( 12), 880-886.
[79] Suzuki A., Josselyn S. A., Frankland P. W., Masushige S., Silva A. C., & Kida S . (2004). Memory reconsolidation and extinction have distinct temporal and biochemical signatures. The Journal of Neuroscience, 24( 20), 4787-4795.
[80] Taylor J.., &Torregrossa M.M . (2015). Pharmacological disruption of maladaptive memory. Handbook of Experimental Pharmacology, 228, 381-415.
[81] Thome J., Koppe G., Hauschild S., Liebke L., Schmahl C., Lis S., & Bohus M . (2016). Modification of fear memory by pharmacological and behavioural interventions during reconsolidation. Plos One, 11( 8), e0161044.
[82] Treanor M., Brown L. A., Rissman J., & Craske M. G . (2017). Can memories of traumatic experiences or addiction be erased or modified? A critical review of research on the disruption of memory reconsolidation and its applications. Perspectives on Psychological Science, 12( 2), 290-305.
[83] Vaiva G., Ducrocq F., Jezequel K., Averland B., Lestavel P., Brunet A., & Marmar C. R . (2003). Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma. Biological Psychiatry, 54( 9), 947-949.
[84] Warren V. T., Anderson K. M., Kwon C., Bosshardt L., Jovanovic T., Bradley B., & Norrholm S. D . (2014). Human fear extinction and return of fear using reconsolidation update mechanisms: The contribution of on-line expectancy ratings. Neurobiology of Learning and Memory, 113, 165-173.
[85] Wood N. M., Rosasco M. L., Suris A. M., Spring J. D., Marin M. F., Lasko N. B., … Pitman R. K . (2015). Pharmacological blockade of memory reconsolidation in posttraumatic stress disorder: Three negative psychophysiological studies. Psychiatry Research, 225( 1-2), 30-39.
[86] Xue Y. X., Luo Y. X., Wu P., Shi H. S., Xue L. F., Chen C., … Lu L . (2012). A memory retrieval-extinction procedure to prevent drug craving and relapse. Science, 336( 6078), 241-245.
[87] Zlomuzica A., Dere D., Machulska A., Adolph D., Dere E., & Margraf J . (2014). Episodic memories in anxiety disorders: Clinical implications. Frontiers in Behaviour Neuroscience, 8, 131.
[88] Zubedat S. &Akirav I., (2017). The involvement of cannabinoids and mTOR in the reconsolidation of an emotional memory in the hippocampal-amygdala-insular circuit. European Neuropsychopharmacology, 27( 4), 336-349.
[1] CAOYANG Jingwen,LI Junjiao,CHEN Wei,YANG Yong,HU Yanjian,ZHENG Xifu. The effect of retrieval intervention paradigm to conditioned fear extinction and its neural mechanism[J]. Advances in Psychological Science, 2019, 27(2): 268-277.
[2] WANG Hongbo; ZHU Xiangru. Effect of noradrenergic regulation on prevention and treatment of posttraumatic stress disorder[J]. Advances in Psychological Science, 2016, 24(6): 923-933.
[3] ZENG Xiangxing; DU Juan; WANG Kaixin; ZHENG Xifu. Temporal Dynamic and Biological Mechanism of Memory Reconsolidation[J]. Advances in Psychological Science, 2015, 23(4): 582-590.
[4] ZENG Xiangxing;XIANG Yanhui;DU Juan;ZHENG Xifu. A Retrieval-Extinction Paradigm to Treat Conditioned Fear Memory[J]. Advances in Psychological Science, 2014, 22(3): 431-438.
[5] WANG Hong-Bo; AN Xian-Li; LI You-Hong; ZHENG Xi-Geng. Analysis of the Factors Influencing Intervention of Conditioned Fear Memory[J]. , 2010, 18(05): 718-724.
[6] WU Yan;LI Yong-Hui;SUI Nan. Memory Reconsolidation and Its Potential Neurobiological Mechanism[J]. , 2009, 17(04): 699-705.
[7] AN Xian-Li ;WANG Wen-Zhonga;ZHENG Xi-Geng. Reasons Block Extinction of Conditioned Fear Memory[J]. , 2009, 17(01): 126-131.
Full text



Copyright © Advances in Psychological Science
Support by Beijing Magtech