题名

A Tale of Two Engrams: Roles of the Hippocampus and Amygdala in Contextual Fear Conditioning

并列篇名

雙痕記:海馬與杏仁核在情境恐懼制約中的角色

DOI

10.6129/CJP.201912_61(4).0004

作者

梁庚辰(Keng-Chen Liang);陳德祐(Der-Yow Chen);張世達(Shih-Dar Chang)

关键词

conditioned reflex ; configural memory ; context representation ; functional localization ; shock association ; 條件反射 ; 組態記憶 ; 情境表徵 ; 腦功能區位化 ; 電擊聯結

期刊名称

中華心理學刊

卷期/出版年月

61卷4期(2019 / 12 / 01)

页次

321 - 340

内容语文

英文

中文摘要

This review focuses on the research for physiological psychology of fear memory done in our laboratory, specifically on the roles of the amygdala and hippocampus in contextual fear conditioning. We present findings to suggest that the hippocampus is involved not only in representing the context of conditioning but also in associating it to an electric shock. The hippocampal GABAergic and cholinergic systems mediated the context representation and context-shock association respectively. These findings demand revising the prevailing model of contextual fear conditioning: In short, the brain may store two engrams for the context-shock association in such conditioning, one relying on the amygdala for a simple reflexive association of CS and US, while the other on the hippocampus for combinatorial binding of all cues in a conditioning episode. These findings, in relating to those from the local and other laboratories, invite re-thinking on the concept of functional localization in the brain.

英文摘要

此論文回顧本生心實驗室對杏仁核與海馬在情境恐懼學習中不同角色的研究結果。我們發現海馬不僅參與情境表徵的形成,也參與情境與電擊的聯結,這有別於目前流行模式之預測。這兩個功能分別由海馬內的伽瑪胺基丁酸與乙醯膽鹼系統負責。易言之,對於情境恐懼制約學習,腦中會形成兩個情境電擊聯結表徵:在杏仁核形成簡單的CS-US反射式聯結以支援快速反應,而在海馬形成一整合式的組態表徵以支援靈活因應。這一恐懼聯結有雙重記憶表徵的發現,在合併考量本地與國際的生心研究成果下,促使吾人重新思考生理心理學中所謂腦功能區位化的意涵。

主题分类 社會科學 > 心理學
参考文献
  1. Hung, H. C.,Hsieh, C. J.,Li, J. S.(2015).The medial prefrontal cortex in rats contributes to the encoding process of episodic-like memory.Chinese Journal of Psychology,57,109-120.
    連結:
  2. Liang, K. C.(2009).Involvement of the amygdala and its connected structures in formation and expression of inhibitory avoidance memory: Issues and implications.Chinese Journal of Physiology,52,196-214.
    連結:
  3. Shen, Y. L.,Liao, R. M.(2007).The effects of acute stress on conditioned place preference.Chinese Journal of Psychology,49,351-363.
    連結:
  4. Berger, T. W.,Alger, B.,Thompson, R. F.(1976).Neuronal substrate of classical conditioning in the hippocampus.Science,192,483-485.
  5. Blanchard, R. J.,Blanchard, D. C.(1969).Crouching as an index of fear.Journal of Comparative Physiological Psychology,67,370-375.
  6. Bliss, T. V. P.,Lomo, T.(1973).Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the performant path.The Journal of Physiology,232,331-356.
  7. Cahill, L.,Weinberger, N. M.,Roozendaal, B.,McGaugh, J. L.(1999).Is the amygdala a locus of "conditioned fear"? Some questions and caveats.Neuron,23,227-228.
  8. Chai, S. N.,White, N. M.(2004).Effects of fimbria-fornix, hippocampus, and amygdala lesions on discrimination between proximal locations.Behavioral Neuroscience,118,770-784.
  9. Chang, C. H.,Liang, K. C.,Yen, C. T.(2005).Inhibitory avoidance learning altered ensemble activity of amygdaloid neurons in rats.European Journal of Neuroscience,21,210-218.
  10. Chang, C. Y.,Chen, Y. W.,Wang, T. W.,Lai, W. S.(2016).Akting up in the GABA hypothesis of schizophrenia: Akt1 deficiency modulates GABAergic functions and hippocampus-dependent functions.Scientific Reports,6,33095.
  11. Chang, S. D.,Chen, D. Y.,Liang, K. C.(2008).Infusion of lidocaine into the dorsal hippocampus before or after the electric shock training phase impaired conditioned freezing in a two-phase training task of contextual fear conditioning.Neurobiology of Learning and Memory,89,95-105.
  12. Chang, S. D.,Liang, K. C.(2017).The hippocampus integrates context and shock into a configural memory in contextual fear conditioning.Hippocampus,27,145-155.
  13. Chang, S. D.,Liang, K. C.(2012).Roles of hippocampal GABAA and muscarinic receptors in consolidation of context memory and context-shock association in contextual fear conditioning: A double dissociation study.Neurobiology of Learning and Memory,98,17-24.
  14. Chao, O. Y.,Huston, J. P.,Li, J. S.,Wang, A. L.,de Souza Silva, M. A.(2016).The medial prefrontal cortex-lateral entorhinal cortex circuit is essential for episodic like memory and associative object recognition.Hippocampus,26,633-645.
  15. Chen, D. Y.,Ho, S. H.,Liang, K. C.(2000).Startle responses to electric shocks: Measurement of shock sensitivity and effects of morphine, buspirone and brain lesions.Chinese Journal of Physiology,43,35-47.
  16. Chen, Y. C.,Ma, Y. L.,Lin, C. H.,Cheng, S. J.,Hsu, W. L.,Lee, E. H.(2017).Galectin-3 negatively regulates hippocampus-dependent memory formation through inhibition of integrin signaling and galectin-3 phosphorylation.Frontiers in Molecular Neuroscience,10,217.
  17. Cherng, C. G.,Lin, P. S.,Chuang, J. Y.,Chang, W. T.,Lee, Y. S.,Kao, G. S.,Yu, L.(2010).Presence of conspecifics and their odor-impregnated objects reverse stress-decreased neurogenesis in mouse dentate gyrus.Journal of Neurochemistry,112,1138-1146.
  18. Chien, W. L.,Liang, K. C.,Fu, W. M.(2008).Enhancement of active shuttle avoidance response by the NO-cGMP-PKG activator YC-1.European Journal of Pharmacology,590,233-240.
  19. Chien, W. L.,Liang, K. C.,Teng, C. M.,Kuo, S. C.,Lee, F. Y.,Fu, W. M.(2003).Enhancement of long-term potentiation by a potent nitric oxide-guanylyl cyclase activation YC-1.Molecular Pharmacology,63,1322-1328.
  20. Cohen, D. H.(1985).Some organizational principles of a vertebrate conditioning pathway: Is memory a distributed property?.Memory systems of the brain,New York:
  21. Danjo, T.,Toyoizumi, T.,Fujisawa, S.(2018).Spatial representations of self and other in the hippocampus.Science,359,213-218.
  22. de Almeida, M. A. M. R.,Izquierdo, I.(1984).Effect of the intraperitoneal and intra-cerebroventricular administration of ACTH, epinephrine, or β-endorphin on retrieval of an inhibitory avoidance task in rats.Behavioral and Neural Biology,40,119-122.
  23. Eichenbaum, H.(1999).The hippocampus and mechanisms of declarative memory.Behavioural Brain Research,103,123-133.
  24. Eichenbaum, H.(2000).A cortical-hippocampal system for declarative memory.Nature Review of Neurosciences,1,41-50.
  25. Eichenbaum, H.(1996).Is the rodent hippocampus just for ‘place’?.Current Opinion in Neurobiology,6,187-195.
  26. Fanselow, M. S.(1990).Factors governing one-trial contextual conditioning.Animal Learning Behavior,18,264-270.
  27. Fanselow, M. S.,LeDoux, J. E.(1999).Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala.Neuron,23,229-232.
  28. Farr, S. A.,Flood, J. F.,Morley, J. E.(2000).The effect of cholinergic, GABAergic, serotonergic, and glutamatergic receptor modulation on posttrial memory processing in the hippocampus.Neurobiology of Learning and Memory,73,150-167.
  29. Fendt, M.,Fanselow, M. S.(1999).The neuroanatomical and neurochemic a l basis of conditioned fear.Neuroscience & Biobehavioral Review,23,43-760.
  30. Flaherty, C. F.(1996).Incentive relativity.Cambridge, UK:Cambrdige University Press.
  31. Fortin, N. J.,Wright, S. P.,Eichenbaum, H.(2004).Recollection-like memory retrieval in rats is dependent on the hippocampus.Nature,431,188-191.
  32. Gold, P. E.(Ed.),Greenough, W. T.(Ed.)(2001).Memory consolidation.Washington DC:American Psychological Association.
  33. Gold, P. E.,McCarty, R.(1981).Plasma catecholamines: changes after footshock and seizure-producing frontal cortex stimulation.Behavioral & Neural Biology,31,247-260.
  34. Gold, P. E.,van Buskirk, R.(1975).Facilitation of time-dependent memory processes with post-trial epinephrine injection.Behavioral Biology,13,145-153.
  35. Hall, J.,Thomas, K. L.,Everitt, B. J.(2000).Rapid and selective induction of BDNF expression in the hippocampus during contextual learning.Nature Neuroscience,3,533-535.
  36. Hasselmo, M. E.(2006).The role of acetylcholine in learning and memory.Current Opinion in Neurobiology,16,710-715.
  37. Hebb, D. O. (1949). The organization of behavior. New York: Wiley and Sons.
  38. Hsiao, F. C.,Liao Y. H.,Tsai, L. L.(2013).Differential effects of retinal degeneration on sleep and wakefulness responses to short light-dark cycles in albino mice.Neuroscience,248,459-468.
  39. Hsiao, S. S.,Isaacson, R.(1971).Learning of food and water positions by hippocampus damaged rats.Physiology & Behavior,6,81-83.
  40. Hu, S. S. J.,Liu Y. W.,Yu, L.(2015).Medial prefrontal cannabinoid CB1 receptors modulate consolidation and extinction of cocaine-associated memory in mice.Psychopharmacology,232,1803-1815.
  41. Huang, A. C.,Shyu, B. C.,Hsiao, S.,Chen, T. C.,He, A. B.(2013).Neural substrates of fear conditioning, extinction, and spontaneous recovery in passive avoidance learning: a c-fos study in rats.Behavioural Brain Research,237,23-31.
  42. Huang, C. H.,Chiang, Y. W.,Liang, K. C.,Thompson, R. F.,Liu, I. Y.(2010).Extrra-cellular signal regulated kinase 1/2 (ERK) activated in the hippocampal CA1 neurons is critical for retrieval of auditory trace fear memory.Brain Research,1326,143-153.
  43. Huff, N. C.,Frank, M.,Wright-Hardesty, K.,Sprunger, D.,Matus-Amat, P.,Higgins, E.,Rudy, J. W.(2006).Amygdala regulation of immediate early gene expression in the hippocampus induced by contextual fear conditioning.Journal of Neuroscience,26,1616-1623.
  44. Ikegaya, Y.,Saito, H.,Abe, K.(1996).The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo.European Journal of Neuroscience,8,1833-1839.
  45. Ikonen, S.,McMahan, R.,Gallagher, M.,Eichenbaum, H.,Tanila H.(2002).Cholinergic system regulation of spatial representation by the hippocampus.Hippocampus,12,386-397.
  46. Kitamura, T.,Ogawa, S. K.,Roy, D. S.,Okuyama, T.,Morrissey, M. D.,Smith, L. M.,Tonegawa, S.(2017).Engrams and circuits crucial for systems consolidation of a memory.Science,356,73-78.
  47. Knowlton, B. J.,Squire, L. R.(1993).The learning of categories: parallel brain systems for item memory and category knowledge.Science,262,1747-1749.
  48. Konorski, J.(1976).Integrative activity of the brain.Chicago:University of Chicago Press.
  49. Kuo, C. C.,Chiou, R. J.,Liang, K. C.,Yen, C. T.(2009).Differential involvement of anterior cingulate and primary sensorimotor cortices in sensory and affective functions of pain.Journal of Neurophysiology,101,1201-1210.
  50. Lashley, K.(1950).In search of the engram.Society of Experimental Biology Symposium,4,454-482.
  51. Leutgeb, S.,Mizumori, S. J. Y.(1999).Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations.Journal of Neuroscience,19,6661-6672.
  52. Li, J. S.,Chao, Y. S.(2008).Electrolytic lesions of dorsal CA3 impair episodic-like memory in rats.Neurobiology of Learning and Memory,89,192-198.
  53. Li, J. S.,Hsiao, K. Y.,Chen, W. M.(2011).Effects of medial prefrontal cortex lesions in rats on the what-where-when memory of a fear conditioning event.Behavioural Brain Research,218,94-98.
  54. Li, K. C.,Li, J. S.(2013).Conditioned taste aversion as instrumental punishment.Journal of Experimental Psychology: Animal Behavior Process,39,294-297.
  55. Liang, K. C.(2006).Neural circuitry involved in avoidance learning and memory: The amygdala and beyond.Progress in psychological science around the world, vol. 1: Neural, cognitive and developmental issues,Hove, UK:
  56. Liang, K. C.(1999).Neural mechanism underlying affective memory of the inhibitory avoidance response in rats.Chinese Journal of Psychology,41,213-220.
  57. Liang, K. C.,Hsu, C. H.(1975).The role of taste in salt homeostasis in rats.Chinese Journal of Psychology,17,151-156.
  58. Liang, K. C.,Hu, S. J.,Chang, S. C.(1996).Formation and retrieval of inhibitory avoidance memory: Differential roles of glutamate receptors in the amygdala and medial prefrontal cortex.Chinese Journal Physiology,39,155-166.
  59. Liang, K. C.,McGaugh, J. L.,Martinez, J. L., Jr,Jensen, R. A.,Vasquez, B. J.,Messing, R. B.(1982).Posttraining amygdaloid lesions impair retention of an inhibitory avoidance response.Behavioural Brain Research,4,237-249.
  60. Liang, K. C.,Yen, Y. C.,Chang, S. D.,Chen, D. Y.(2005).Epinephrine enhances latent learning in an inhibitory avoidance task: involvement of the amygdaloid influence on the hippocampus.meeting of Society for Neuroscience,Washington, DC:
  61. Liao, R. M.,Chuang, F. J.(2003).Differential effects of diazepam infused into the amygdala and hippocampus on negative contrast.Pharmacology, Biochemistry and Behavior,74,953-960.
  62. Liao, W. L.(2018).Psychomotor dysfunction in Rett syndrome: insights into the neurochemical and circuit roots.Developmental Neurobiology,11,1-9.
  63. Liddell, H. S. (1934). The comparative physiology of the conditioned motor reflex based on experiments with the pig, dog, sheep, goat and rabbit. Baltimore: Johns Hopkins Press. doi: 10.1037/11453-009
  64. Maren, S.(2001).Neurobiology of Pavlovian fear conditioning.Annual Review Neuroscience,24,897-931.
  65. Maren, S.,Fanselow, M. S.(1997).Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats.Neurobiology of Learning and Memory,67,142-149.
  66. Maren, S.,Hobin, J. A.(2007).Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala.Learning and Memory,14,318-324.
  67. Miller, D. P.,Steinmetz, J. E.(1997).Hippocampal activity during classical discrimination-Reversal eyeblink conditioning in rabbits.Behavioral Neuroscience,111,70-79.
  68. Mishra, A.,Cheng, C. H.,Lee, W. C.,Tsai, L. L.(2009).Proteomic changes in the hypothalamus and retroperitoneal fat from male F344 rats subjected to repeated light-dark shifts.Proteomics,9,4017-4028.
  69. Moita, M. A. P.,Rosis, S.,Zhou, Y.,LeDoux, J. E.,Blair, H. T.(2004).Putting fear in its place: remapping of hippocampal place cells during fear conditioning.Journal of Neuroscience,24,7015-7023.
  70. Nader, K.,Schafe, G. E.,LeDoux, J. E.(2000).Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval.Nature,406,722-726.
  71. O’Reilly, R. C,McClelland, J. L.(1994).Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off.Hippocampus,4,661-682.
  72. Omer, D. B.,Maimon, S. R.,Las, L.,Ulanovsky, N.(2018).Social place-cells in the bat hippocampus.Science,359,218-224.
  73. Pavlov, I. (1927). Conditioned reflexes. London: Oxford University Press.
  74. Phillips, R. G.,LeDoux, J. E.(1992).Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.Behavioral Neuroscience,106,274-285.
  75. Ray, W. J.(2013).Evolutionary psychology: Neuroscience perspectives concerning human behavior and experience.London, UK:Sage Publications.
  76. Rudy, J. W.,O’Reilly, R. C.(1999).Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus.Behavioral Neuroscience,113,867-880.
  77. Scoville, W. B.,Milner, B.(1957).Loss of recent memory after bilateral hippocampal lesions.Journal of Neurology, Neurosurgery, and Psychiatry,20,1-11.
  78. Sloman, S. A.(1996).The empirical case for two systems of reasoning.Psychological Bulletin,119,3-22.
  79. Solomon, P. R.,Vander Schaaf, E. R.,Thompson, R. F.,Weisz, D. J.(1986).Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response.Behavioral Neuroscience,100,729-744.
  80. Sporns, O.,Tononi, G.,Edelman, G. M.(2000).Connectivity and complexity: the relationship between neuroanatomy and brain dynamics.Neural Networks,13,909-922.
  81. Squire, L. R.(2004).Memory systems of the brain: A brief history and current perspective.Neurobiology of Learning and Memory,82,171-177.
  82. Thompson, R. F.(2005).In search of memory traces.Annual Review of Psychology,56,1-23.
  83. Tonegawa, S.,Morrissey, M. D.,Kitamura, T.(2017).The role of engram cells in the systems consolidation of memory.Nature Neuroscience Reviews,18,485-498.
  84. Tzeng, W. Y.,Cherng, C. F.,Wang, S. W.,Yu, L.(2016).Familiar companions diminish cocaine conditioning and attenuate cocaine-stimulated dopamine release in the nucleus accumbens.Behavioral Brain Research,306,146-153.
  85. Tzeng, W. Y.,Cherng, C. G.,Yu, L.,Wang, C. Y.(2017).Basolateral amygdalar D2 receptor activation is required for the companions-exerted suppressive effect on the cocaine conditioning.Neurobiology of Learning and Memory,137,48-55.
  86. Tzeng, W. Y.,Chuang, J. Y.,Lin, L. C.,Cherng, C. G.,Lin, K. Y.,Chen, L. H.,Yu, L.(2013).Companions reverse stressor-induced decreases in neurogenesis and cocaine conditioning possibly by restoring BDNF and NGF levels in dentate gyrus.Psychoneuroendocrinology,38,425-437.
  87. von Hertzen, L. S. J.,Giese K. P.(2005).Memory reconsolidation engages only a subset of immediateearly genes induced during consolidation.Journal of Neuroscience,25,1935-1942.
  88. Wang, F. B.,Liao, Y. H.,Wang, Y. C.(2017).Vagal nerve endings in visceral pleura and triangular ligaments of the rat lung.Journal of Anatomy,230,303-314.
  89. Wang, R. Y.,Phang, R. Z.,Hsu, P. H.,Wang, W. H.,Huang, H. T.,Liu, I. Y.(2013).In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning.Hippocampus,23,625-633.
  90. Weng, J. C.,Tikhonova, M. A.,Chen, J. H.,Shen, M. S.,Meng, W. Y.,Chang, Y. T.,Ho, Y. J.(2016).Ceftriaxone prevents the neurodegeneration and decreased neurogenesis seen in a Parkinson's disease rat model: an immunohistochemical and MRI study.Behavioral Brain Research,305,126-139.
  91. White, N. M.,Chai, S. C.,Hamdani, S.(2005).Learning the morphine conditioned cue preference: Cue configuration determines effects of lesions.Pharmacology, Biochemistry and Behavior,81,786-796.
  92. White, N. M.,McDonald, R. J.(2002).Multiple parallel memory systems in the brain of the rat.Neurobiology of Learning and Memory,77,125-184.
  93. Wiltgen, B. J.,Sanders, M. J.,Anagnostaras, S. G.,Sage, J. R.,Fanselow, M. S.(2006).Context fear learning in the absence of the hippocampus.Journal of Neuroscience,26,5484-5491.
  94. Wood, E. R.,Dudchenko, P. A.,Eichenbaum, H.(1999).The global record of memory in hippocampal neuronal activity.Nature,397,613-616.
  95. Yang, F. C.,Liang, K. C.(2014).Interaction of the dorsal hippocampus, medial prefrontal cortex and nucleus accumbens in formation of fear memory: Difference in avoidance learning and contextual fear conditioning.Neurobiology of Learning and Memory,112,186-194.
  96. Yang, Y. P.,Liang, K. C.(2012).Region specific c-Fos expression in formation and expression of inhibitory avoidance memory.meeting of Society for Neuroscience,New Orleans, LA:
被引用次数
  1. 趙軒甫,姜忠信,姜定宇,林佳樺,李思賢(2019)。中華心理學六十週年:創新與超越。中華心理學刊,61(4),i-vii。