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Neuroimaging and intervening in memory reconsolidation of human drug addiction

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Abstract

Reconsolidation refers to memory reprocessing when consolidated memory is being recalled and restored. Importantly, as memory is being recalled, it could further modify past memories. Memory reconsolidation has been identified as a critical role in various types of mental disorders, in particular drug addiction. In this review, we first review earlier studies related to reconsolidation. Secondly, we characterize memory reconsolidation processing in human brain via neuroimaging studies. Then we focus on the role of reconsolidation and reconsolidation-based interventions in drug addiction. Finally, we highlight the potentials of combining reconsolidation-based interventions and neuroimaging techniques as a therapeutic tool in drug addiction.

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References

  1. Kandel E R, Dudai Y, Mayford M R. The molecular and systems biology of memory. Cell, 2014, 157: 163–186

    Article  Google Scholar 

  2. Nader K, Hardt O. A single standard for memory: the case for reconsolidation. Nat Rev Neurosci, 2009, 10: 224–234

    Article  Google Scholar 

  3. Elsey J W B, van Ast V A, Kindt M. Human memory reconsolidation: a guiding framework and critical review of the evidence. Psychol Bull, 2018, 144: 797–848

    Article  Google Scholar 

  4. Lee J L C, Nader K, Schiller D. An update on memory reconsolidation updating. Trends Cogn Sci, 2017, 21: 531–545

    Article  Google Scholar 

  5. Sandrini M, Cohen L G, Censor N. Modulating reconsolidation: a link to causal systems-level dynamics of human memories. Trends Cogn Sci, 2015, 19: 475–482

    Article  Google Scholar 

  6. Sorg B A. Reconsolidation of drug memories. Neurosci Biobehaval Rev, 2012, 36: 1400–1417

    Article  Google Scholar 

  7. Cadet J L, Bisagno V, Milroy C M. Neuropathology of substance use disorders. Acta Neuropathol, 2014, 127: 91–107

    Article  Google Scholar 

  8. Monfils M H, Holmes E A. Memory boundaries: opening a window inspired by reconsolidation to treat anxiety, trauma-related, and addiction disorders. Lancet Psychiatry, 2018, 5: 1032–1042

    Article  Google Scholar 

  9. Schwabe L, Nader K, Pruessner J C. Reconsolidation of human memory: brain mechanisms and clinical relevance. Biol Psychiatry, 2014, 76: 274–280

    Article  Google Scholar 

  10. Xue Y X, Luo Y X, Wu P, et al. A memory retrieval-extinction procedure to prevent drug craving and relapse. Science, 2012, 336: 241–245

    Article  Google Scholar 

  11. Germeroth L J, Carpenter M J, Baker N L, et al. Effect of a brief memory updating intervention on smoking behavior: a randomized clinical trial. JAMA Psychiatry, 2017, 74: 214–223

    Article  Google Scholar 

  12. Dudai Y, Karni A, Born J. The consolidation and transformation of memory. Neuron, 2015, 88: 20–32

    Article  Google Scholar 

  13. Misanin J R, Miller R R, Lewis D J. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science, 1968, 160: 554–555

    Article  Google Scholar 

  14. Schneider A M, Sherman W. Amnesia: a function of the temporal relation of footshock to electroconvulsive shock. Science, 1968, 159: 219–221

    Article  Google Scholar 

  15. Lewis D J, Bregman N J. Source of cues for cue-dependent amnesia in rats. J Comp Physiol Psychol, 1973, 85: 421–426

    Article  Google Scholar 

  16. Lewis D J, Bregman N J, Mahan J J. Cue-dependent amnesia in rats. J Comp Physiol Psychol, 1972, 81: 243–247

    Article  Google Scholar 

  17. Nader K, Schafe G E, Le Doux J E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature, 2000, 406: 722–726

    Article  Google Scholar 

  18. Debiec J, LeDoux J E, Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron, 2002, 36: 527–538

    Article  Google Scholar 

  19. Rose J K, Rankin C H. Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. J Neurosci, 2006, 26: 11582–11587

    Article  Google Scholar 

  20. Schiller D, Monfils M H, Raio C M, et al. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature, 2010, 463: 49–53

    Article  Google Scholar 

  21. Walker M P, Brakefield T, Hobson J A, et al. Dissociable stages of human memory consolidation and reconsolidation. Nature, 2003, 425: 616–620

    Article  Google Scholar 

  22. Ogawa S, Tank D W, Menon R, et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA, 1992, 89: 5951–5955

    Article  Google Scholar 

  23. Goense J, Merkle H, Logothetis N K. High-resolution fMRI reveals laminar differences in neurovascular coupling between positive and negative BOLD responses. Neuron, 2012, 76: 629–639

    Article  Google Scholar 

  24. Agren T, Engman J, Frick A, et al. Disruption of reconsolidation erases a fear memory trace in the human amygdala. Science, 2012, 337: 1550–1552

    Article  Google Scholar 

  25. Björkstrand J, Agren T, Åhs F, et al. Think twice, it’s all right: long lasting effects of disrupted reconsolidation on brain and behavior in human long-term fear. Behavioural Brain Res, 2017, 324: 125–129

    Article  Google Scholar 

  26. Feng P, Zheng Y, Feng T. Spontaneous brain activity following fear reminder of fear conditioning by using resting-state functional MRI. Sci Rep, 2015, 5: 16701–16711

    Article  Google Scholar 

  27. Han J H, Kushner S A, Yiu A P, et al. Selective erasure of a fear memory. Science, 2009, 323: 1492–1496

    Article  Google Scholar 

  28. Monfils M H, Cowansage K K, Klann E, et al. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science, 2009, 324: 951–955

    Article  Google Scholar 

  29. Cheng D T, Richards J, Helmstetter F J. Activity in the human amygdala corresponds to early, rather than late period autonomic responses to a signal for shock. Learn Mem, 2007, 14: 485–490

    Article  Google Scholar 

  30. Knight D C, Nguyen H T, Bandettini P A. The role of the human amygdala in the production of conditioned fear responses. Neuroimage, 2005, 26: 1193–1200

    Article  Google Scholar 

  31. Schwabe L, Nader K, Wolf O T, et al. Neural signature of reconsolidation impairments by propranolol in humans. Biol Psychiatry, 2012, 71: 380–386

    Article  Google Scholar 

  32. Mahabir M, Tucholka A, Shin L M, et al. Emotional face processing in post-traumatic stress disorder after reconsolidation impairment using propranolol: a pilot fMRI study. J Anxiety Disorders, 2015, 36: 127–133

    Article  Google Scholar 

  33. Richardson M P, Strange B A, Dolan R J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat Neurosci, 2004, 7: 278–285

    Article  Google Scholar 

  34. Kindt M, Soeter M, Vervliet B. Beyond extinction: erasing human fear responses and preventing the return of fear. Nat Neurosci, 2009, 12: 256–258

    Article  Google Scholar 

  35. Przybyslawski J, Roullet P, Sara S J. Attenuation of Emotional and Nonemotional Memories after their Reactivation: Role of β Adrenergic Receptors. J Neurosci, 1999, 19: 6623–6628

    Article  Google Scholar 

  36. Shin L M, Wright C I, Cannistraro P A, et al. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry, 2005, 62: 273–281

    Article  Google Scholar 

  37. Schiller D, Kanen J W, LeDoux J E, et al. Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proc Natl Acad Sci USA, 2013, 110: 20040–20045

    Article  Google Scholar 

  38. Feng P, Zheng Y, Feng T. Resting-state functional connectivity between amygdala and the ventromedial prefrontal cortex following fear reminder predicts fear extinction. Soc Cogn Affect Neurosci, 2016, 11: 991–1001

    Article  Google Scholar 

  39. Bouton M E. Context and behavioral processes in extinction. Learn Memory, 2004, 11: 485–494

    Article  Google Scholar 

  40. Khalaf O, Resch S, Dixsaut L, et al. Reactivation of recall-induced neurons contributes to remote fear memory attenuation. Science, 2018, 360: 1239–1242

    Article  Google Scholar 

  41. Visser R M, Lau-Zhu A, Henson R N, et al. Multiple memory systems, multiple time points: how science can inform treatment to control the expression of unwanted emotional memories. Philos Trans R Soc Lond B Biol Sci, 2018, 373: 1742

    Article  Google Scholar 

  42. Pare D, Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr Opin Neurobiol, 2012, 22: 717–723

    Article  Google Scholar 

  43. Milad M R, Wright C I, Orr S P, et al. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry, 2007, 62: 446–454

    Article  Google Scholar 

  44. Sotres-Bayon F, Quirk G J. Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol, 2010, 20: 231–235

    Article  Google Scholar 

  45. Dayan E, Censor N, Buch E R, et al. Noninvasive brain stimulation: from physiology to network dynamics and back. Nat Neurosci, 2013, 16: 838–844

    Article  Google Scholar 

  46. Sandrini M, Caronni A, Corbo M. Modulating reconsolidation with non-invasive brain stimulation-where we stand and future directions. Front Psychol, 2018, 9: 1430

    Article  Google Scholar 

  47. Grossman N, Bono D, Dedic N, et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell, 2017, 169: 1029–1041

    Article  Google Scholar 

  48. Sandrini M, Censor N, Mishoe J, et al. Causal role of prefrontal cortex in strengthening of episodic memories through reconsolidation. Curr Biol, 2013, 23: 2181–2184

    Article  Google Scholar 

  49. Censor N, Dayan E, Cohen L G. Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories. Cortex, 2014, 58: 281–288

    Article  Google Scholar 

  50. Manenti R, Cotelli M, Robertson I H, et al. Transcranial brain stimulation studies of episodic memory in young adults, elderly adults and individuals with memory dysfunction: a review. Brain Stimul, 2012, 5: 103–109

    Article  Google Scholar 

  51. Sandrini M, Cappa S F, Rossi S, et al. The role of prefrontal cortex in verbal episodic memory: rTMS evidence. J Cogn Neurosci, 2003, 15: 855–861

    Article  Google Scholar 

  52. Censor N, Dimyan M A, Cohen L G. Modification of existing human motor memories is enabled by primary cortical processing during memory reactivation. Curr Biol, 2010, 20: 1545–1549

    Article  Google Scholar 

  53. Javadi A H, Cheng P. Transcranial direct current stimulation (tDCS) enhances reconsolidation of long-term memory. Brain Stimul, 2013, 6: 668–674

    Article  Google Scholar 

  54. Sandrini M, Brambilla M, Manenti R, et al. Noninvasive stimulation of prefrontal cortex strengthens existing episodic memories and reduces forgetting in the elderly. Front Aging Neurosci, 2014, 6: 289

    Article  Google Scholar 

  55. Gagnon G, Blanchet S, Grondin S, et al. Paired-pulse transcranial magnetic stimulation over the dorsolateral prefrontal cortex interferes with episodic encoding and retrieval for both verbal and non-verbal materials. Brain Res, 2010, 1344: 148–158

    Article  Google Scholar 

  56. Gagnon G, Schneider C, Grondin S, et al. Enhancement of episodic memory in young and healthy adults: a paired-pulse TMS study on encoding and retrieval performance. Neurosci Lett, 2011, 488: 138–142

    Article  Google Scholar 

  57. Javadi A H, Walsh V. Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimul, 2012, 5: 231–241

    Article  Google Scholar 

  58. Drevets W C, Gautier C, Price J C, et al. Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry, 2001, 49: 81–96

    Article  Google Scholar 

  59. Hellemans K G C, Everitt B J, Lee J L C. Disrupting reconsolidation of conditioned withdrawal memories in the basolateral amygdala reduces suppression of heroin seeking in rats. J Neurosci, 2006, 26: 12694–12699

    Article  Google Scholar 

  60. Kenny P J, Chen S A, Kitamura O, et al. Conditioned withdrawal drives heroin consumption and decreases reward sensitivity. J Neurosci, 2006, 26: 5894–5900

    Article  Google Scholar 

  61. Koob G F, Volkow N D. Neurocircuitry of addiction. Neuropsychopharmacol, 2010, 35: 217–238

    Article  Google Scholar 

  62. Robinson T E, Berridge K C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev, 1993, 18: 247–291

    Article  Google Scholar 

  63. Robinson T E, Berridge K C. Incentive-sensitization and addiction. Addiction, 2001, 96: 103–114

    Article  Google Scholar 

  64. Chiu C Q, Puente N, Grandes P, et al. Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci, 2010, 30: 7236–7248

    Article  Google Scholar 

  65. Wang W, Dever D, Lowe J, et al. Regulation of prefrontal excitatory neurotransmission by dopamine in the nucleus accumbens core. J Physiol, 2012, 590: 3743–3769

    Article  Google Scholar 

  66. Milton A L, Everitt B J. The psychological and neurochemical mechanisms of drug memory reconsolidation: implications for the treatment of addiction. Eur J Neurosci, 2010, 31: 2308–2319

    Article  Google Scholar 

  67. Tronson N C, Taylor J R. Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci, 2007, 8: 262–275

    Article  Google Scholar 

  68. Rodriguez W A, Rodriguez S B, Phillips M Y, et al. Post-reactivation cocaine administration facilitates later acquisition of an avoidance response in rats. Behavioural Brain Res, 1993, 59: 125–129

    Article  Google Scholar 

  69. Fan H Y, Cherng C G, Yang F Y, et al. Systemic treatment with protein synthesis inhibitors attenuates the expression of cocaine memory. Behavioural Brain Res, 2010, 208: 522–527

    Article  Google Scholar 

  70. Alaghband Y, O’Dell S J, Azarnia S, et al. Retrieval-induced NMDA receptor-dependent Arc expression in two models of cocaine-cue memory. Neurobiol Learn Memory, 2014, 116: 79–89

    Article  Google Scholar 

  71. Lv X F, Sun L L, Cui C L, et al. NAc shell Arc/Arg3.1 protein mediates reconsolidation of morphine CPP by increased GluR1 cell surface expression: activation of ERK-coupled CREB is required. Int J Neuropsychopharmacol, 2015, 18: pyv030

    Article  Google Scholar 

  72. Pavlov P I. Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Ann Neurosci, 2010, 17: 136–141

    Article  Google Scholar 

  73. Finnie P S B, Nader K. The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation. Neurosci Biobehaval Rev, 2012, 36: 1667–1707

    Article  Google Scholar 

  74. Merlo E, Bekinschtein P, Jonkman S, et al. Molecular mechanisms of memory consolidation, reconsolidation, and persistence. Neural Plast, 2015, 2015: 687175

    Article  Google Scholar 

  75. Addis D R, Wong A T, Schacter D L. Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration. Neuropsychologia, 2007, 45: 1363–1377

    Article  Google Scholar 

  76. Wirkner J, Low A, Hamm A O, et al. New learning following reactivation in the human brain: targeting emotional memories through rapid serial visual presentation. Neurobiol Learn Memory, 2015, 119: 63–68

    Article  Google Scholar 

  77. Forcato C, Bavassi L, de Pino G, et al. Differential left hippocampal activation during retrieval with different types of reminders: an fMRI study of the reconsolidation process. PLoS One, 2016, 11: e0151381

    Article  Google Scholar 

  78. Costanzi M, Cannas S, Saraulli D, et al. Extinction after retrieval: effects on the associative and nonassociative components of remote contextual fear memory. Learn Memory, 2011, 18: 508–518

    Article  Google Scholar 

  79. Ishii D, Matsuzawa D, Matsuda S, et al. No erasure effect of retrieval-extinction trial on fear memory in the hippocampus-independent and dependent paradigms. Neurosci Lett, 2012, 523: 76–81

    Article  Google Scholar 

  80. Jones C E, Ringuet S, Monfils M H. Learned together, extinguished apart: reducing fear to complex stimuli. Learn Memory, 2013, 20: 674–685

    Article  Google Scholar 

  81. Hu J C, Wang W Q, Homan P, et al. Reminder duration determines threat memory modification in humans. Sci Rep, 2018, 8: 8848

    Article  Google Scholar 

  82. Isserles M, Shalev A Y, Roth Y, et al. Effectiveness of deep transcranial magnetic stimulation combined with a brief exposure procedure in post-traumatic stress disorder—a pilot study. Brain Stimul, 2013, 6: 377–383

    Article  Google Scholar 

  83. Kaneta T. PET and SPECT imaging of the brain: a review on the current status of nuclear medicine in Japan. Jpn J Radiol, 2020, 38: 343–357

    Article  Google Scholar 

  84. Pan Y, Borragán G, Peigneux P. Applications of functional near-infrared spectroscopy in fatigue, sleep deprivation, and social cognition. Brain Topogr, 2019, 32: 998–1012

    Article  Google Scholar 

  85. Somer E, Allen J, Brooks J, et al. Theta phase-dependent modulation of perception by concurrent transcranial alternating current stimulation and periodic visual stimulation. J Cognitive Neurosci, 2020, 3: 1–11

    Google Scholar 

  86. Song P, Han T, Lin H, et al. Transcranial near-infrared stimulation may increase cortical excitability recorded in humans. Brain Res Bull, 2020, 155: 155–158

    Article  Google Scholar 

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Acknowledgements

This work was supported by National Key Basic Research Program (Grant Nos. 2016YFA0400900, 2018YFC0831101), National Natural Science Foundation of China (Grant Nos. 71942003, 31771221, 61773360, 71874170), School Foundation of Anhui Medical University (Grant Nos. 2019xkj016, XJ201907), National Science Foundation for Young Scientists of China (Grant No. 31900766), Major Project of Philosophy and Social Science Research, Ministry of Education of China (Grant No. 19JZD010), Fundamental Research Funds for the Central Universities of China. A portion of the numerical calculations in this study were performed with the supercomputing system at the Supercomputing Centre of USTC.

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Authors and Affiliations

  1. Department of Psychiatry, The First Affiliated Hospital of Anhui Medical University, Hefei, 230022, China

    Chuan Fan

  2. School of Life Science, Division of Life Science and Medicine, University of Science and Technology of China, Hefei, 230026, China

    Chuan Fan, Yan Cheng, Huixing Gou, Chang Liu, Shengliang Deng, Chialun Liu & Xiaochu Zhang

  3. Department of Neurology, The First Affiliated Hospital of Anhui Medical University, Hefei, 230022, China

    Xianwen Chen

  4. School of Biomedical Engineering, Anhui Medical University, Hefei, 230032, China

    Junjie Bu

  5. CAS Key Laboratory of Brain Function and Disease, University of Science and Technology of China, Hefei, 230026, China

    Xiaochu Zhang

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  1. Chuan Fan
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  2. Yan Cheng
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  3. Huixing Gou
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Correspondence to Junjie Bu or Xiaochu Zhang.

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Fan, C., Cheng, Y., Gou, H. et al. Neuroimaging and intervening in memory reconsolidation of human drug addiction. Sci. China Inf. Sci. 63, 170103 (2020). https://doi.org/10.1007/s11432-019-2847-8

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