Heroes of the engram

Journal of Neuroscience

Volumn 37, Issue 18, 2017, Pages 4647-4657

  Josselyn, Sheena A ^a,b,c,d   Köhler, Stefan ^e,f   Frankland, Paul W ^a,b,c,d  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^e UNIVERSITY OF WESTERN ONTARIO   (Canada)

^f BAYCREST CENTRE FOR GERIATRIC CARE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CEREBELLUM; ENGRAM; HISTORICAL PERIOD; HUMAN; MEMORY; NERVOUS SYSTEM; NEUROPSYCHOLOGY; PRIORITY JOURNAL; PROBLEM BEHAVIOR; SCIENTIST; STIMULUS; TRAINING; BIOLOGICAL MODEL; BRAIN; EVIDENCE BASED MEDICINE; MALE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PHYSIOLOGY; RECALL;

BRAIN; EVIDENCE-BASED MEDICINE; HUMANS; MALE; MEMORY; MENTAL RECALL; MODELS, NEUROLOGICAL; NERVE NET; NEURONAL PLASTICITY;

EID: 85018924761     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0056-17.2017     Document Type: Article

References (116)

1. Bartlett FC (1960) Karl Spencer Lashley, 1890-1958. Biographical Memoirs of Fellows of the Royal Society 5:107-118. CrossRef
2. Beach FA (1961) Karl Spencer Lashley. Washington, DC: National Academy of Sciences.
3. Beolens B, Watkins M, Grayson M (2011) The eponym dictionary of reptiles. Baltimore: Johns Hopkins UP.
4. Berger TW, OrrWB (1983) Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response. Behav Brain Res 8:49-68. CrossRef Medline
5. Berger TW, Thompson RF (1978) Identification of pyramidal cells as the critical elements in hippocampal neuronal plasticity during learning. Proc Natl Acad Sci U S A 75:1572-1576. CrossRef Medline
6. Berger TW, Laham RI, Thompson RF (1980) Hippocampal unit-behavior correlations during classical conditioning. Brain Res 193:229-248. CrossRef Medline
7. Berndt A, Lee SY, Wietek J, Ramakrishnan C, Steinberg EE, Rashid AJ, Kim H, Park S, Santoro A, Frankland PW, Iyer SM, Pak S, Ährlund-Richter S, Delp SL, Malenka RC, Josselyn SA, Carlén M, Hegemann P, Deisseroth K (2016) Structural foundations of optogenetics: determinants of channelrhodopsin ion selectivity. Proc Natl Acad Sci U S A 113:822-829. CrossRef Medline
8. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472. Medline
9. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356. CrossRef Medline
10. Bloedel JR (1993) ‘Involvement in’ versus ‘storage of.' Trends Neurosci 16:451-452; discussion 453-454. Medline
11. Bower JM (1997) Is the cerebellum sensory for motor’s sake, or motor for sensory’s sake: the view from the whiskers of a rat? Prog Brain Res 114:463-496. CrossRef Medline
12. Brown RE (2006) The life and work of Donald Olding Hebb. Acta Neurol Taiwan 15:127-142. Medline
13. Brown RE, MilnerPM (2003) The legacy of Donald O. Hebb: more than the Hebb synapse. Nat Rev Neurosci 4:1013-1019. CrossRef Medline
14. Bruce D (1998) The Lashley-Hull debate revisited. Hist Psychol 1:69-84. CrossRef Medline
15. Carrillo-Reid L, Yang W, Bando Y, Peterka DS, Yuste R (2016) Imprinting and recalling cortical ensembles. Science 353:691-694. CrossRef Medline
16. Chen S, Cai D, Pearce K, Sun PY, Roberts AC, Glanzman DL (2014) Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia. eLife 3:e03896. CrossRef Medline
17. Cooper SJ (2005) Donald O. Hebb’s synapse and learning rule: a history and commentary. Neurosci Biobehav Rev 28:851-874. CrossRef Medline
18. Cowansage KK, Shuman T, Dillingham BC, Chang A, Golshani P, MayfordM (2014) Direct reactivation of a coherent neocortical memory of context. Neuron 84:432-441. CrossRef Medline
19. Denny CA, Kheirbek MA, Alba EL, Tanaka KF, Brachman RA, Laughman KB, Tomm NK, Turi GF, Losonczy A, Hen R (2014) Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron 83:189-201. CrossRef Medline
20. Dias BG, Ressler KJ (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17:89-96. CrossRef Medline
21. Eichenbaum H (2016) Still searching for the engram. Learn Behav 44:209-222. CrossRef Medline
22. ForsdykeDR (2006) Heredity as transmission of information: Butlerian ‘Intelligent Design.' Centaurus 48:133-148. CrossRef
23. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119-130. CrossRef Medline
24. Franz SI (1912) New phrenology. Science 35:321-328. CrossRef Medline
25. Franz SI, Lashley KS (1917) The retention of habits by the rat after destruction of the frontal portion of the cerebrum. Psychobiology 1:3-18.CrossRef
26. Friston K (2002) Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Annu Rev Neurosci 25:221-250. CrossRef Medline
27. Garner AR, Rowland DC, Hwang SY, Baumgaertel K, Roth BL, Kentros C, MayfordM (2012) Generation of a synthetic memory trace. Science 335:1513-1516. CrossRef Medline
28. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322:96-101. CrossRef Medline
29. Gomulicki BR (1953) The development and present status of the trace theory of memory. Br J Psychol Monogr Suppl 29:1-94.
30. Gräff J, Mansuy IM (2008) Epigenetic codes in cognition and behaviour. Behav Brain Res 192:70-87. CrossRef Medline
31. Hamani C, Hodaie M, Chiang J, del Campo M, Andrade DM, Sherman D, Mirski M, Mello LE, Lozano AM (2008) Deep brain stimulation of the anterior nucleus of the thalamus: effects of electrical stimulation on pilocarpine-induced seizures and status epilepticus. Epilepsy Res 78:117-123. CrossRef Medline
32. Hebb DO (1945) Man’s frontal lobes: a critical review. Arch Neurol Psychiatry 54:10-24. CrossRef
33. Hebb DO (1949) The organization of behavior, a neuropsychological theory. New York: Wiley.
34. Hebb DO, Morton NW (1943) The McGill Adult Comprehension Examination:“Verbal situation” and “Picture Anomaly” Series. J Educ Psychol 34:16-25. CrossRef
35. Hebb DO, Penfield W (1940) Human behavior after extensive bilateral removal from the frontal lobes. Arch Neurol Psychiatry 42:421-438.
36. Hebb DO, Williams K (1946) A method of rating animal intelligence. J Gen Psychol 34:59-65. CrossRef Medline
37. Hsiang HL, Epp JR, van den Oever MC, Yan C, Rashid AJ, Insel N, Ye L, Niibori Y, Deisseroth K, Frankland PW, Josselyn SA (2014) Manipulating a “cocaine engram” in mice. J Neurosci 34:14115-14127. CrossRef Medline
38. JosselynSA (2010) Continuing the search for the engram: examining the mechanism of fear memories. J Psychiatry Neurosci 35:221-228. CrossRef Medline
39. Josselyn SA, Köhler S, Frankland PW (2015) Finding the engram. Nat Rev Neurosci 16:521-534. CrossRef Medline
40. Kim H (2011) Neural activity that predicts subsequent memory and forgetting:a meta-analysis of 74 fMRI studies. Neuroimage 54:2446-2461. CrossRef Medline
41. Kim JI, Cho HY, Han JH, Kaang BK (2016) Which neurons will be the engram-activated neurons and/or more excitable neurons? Exp Neurobiol 25:55-63. CrossRef Medline
42. Lashley KS (1933) Integrative functions of the cerebral cortex. Physiol Rev 13:1-42.
43. Lashley KS (1935) Studies of cerebral function in learning: XI. The behavior of the rat in latch-box situations. Comp Psychol Monogr 11:5-42.
44. Lavond DG, Kanzawa SA (2001) Reflections on R. F. Thompson’s discovery of the engram. Engram 1:6-14.
45. Lewis J (1981) Something hidden: a biography of Wilder Penfield. Toronto:Doubleday.
46. Li L, Sanchez CP, Slaughter BD, Zhao Y, Khan MR, Unruh JR, Rubinstein B, Si K (2016) A putative biochemical engram of long-term memory. Curr Biol 26:3143-3156. CrossRef Medline
47. Lincoln JS, McCormick DA, Thompson RF (1982) Ipsilateral cerebellar lesions prevent learning of the classically conditioned nictitating membrane/eyelid response. Brain Res 242:190-193. CrossRef Medline
48. Liu X, Ramirez S, Pang PT, Puryear CB, Govindarajan A, Deisseroth K, Tonegawa S (2012) Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484:381-385. CrossRef Medline
49. Mayford M (2014) The search for a hippocampal engram. Philos Trans R Soc Lond B Biol Sci 369:20130161. CrossRef Medline
50. McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457. CrossRef Medline
51. McConnell JV (1962) Memory transfer through cannibalism in planarians. J Neuropsychiatry Suppl 3:42-48.
52. McConnell JV, Jacobson AL, Kimble DP (1959) The effects of regeneration upon retention of a conditioned response in the planarian. J Comp Physiol Psychol 52:1-5. CrossRef Medline
53. McCormick DA, Thompson RF (1984) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4:2811-2822.Medline
54. McCormick DA, Lavond DG, Clark GA, Kettner RE, Rising CE, Thompson RF (1981) The engram found? Role of the cerebellum in classical conditioning of nictitating membrane and eyelid responses. Bull Psychonom Soc 18:103-105. CrossRef
55. McGarry DB (2009) The Metalogicon of John of Salisbury: a Twelfth-Century defense of the verbal and logical arts of the trivium. Berkeley:University of California.
56. McIntosh AR (1999) Mapping cognition to the brain through neural interactions. Memory 7:523-548. CrossRef Medline
57. Merton RK (1968) The Matthew effect in science: the reward and communication systems of science are considered. Science 159:56-63. CrossRef Medline
58. Milner B (1962) Les troubles de la memoire accompagnant des lesions hippocampiques bilaterales. In Physiologie de l’Hippocampe, ed Passouant P, pp 257-272. Paris: Centre National de la Recherche Scientifique (CNRS).
59. Milner B (1998) Brenda Milner. In: The History of Neuroscience in Autobiography (Squire LR, ed), pp 276-305. San Diego: Academic.
60. Milner PM (1999) Cell assemblies: Whose idea? In: Psycholoquy [online]. http://www.cogsci.ecs.soton.ac.uk/cgi/psyc/newpsy?10.053.
61. Milner PM, Milner B (1996) Donald O. Hebb. Biographical memoirs of Fellows of the Royal Society 42:192-204. CrossRef
62. Moscovitch M (2012) Memory before and after H.M.: an impressionistic historical perspective. In: Epilepsy and memory (Zeman A, Kapur N, Jones-Gotman M, eds), pp 19-50. Oxford: Oxford UP.
63. Moscovitch M, Rosenbaum RS, Gilboa A, Addis DR, Westmacott R, Grady C, McAndrews MP, Levine B, Black S, Winocur G, Nadel L (2005) Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207:35-66. CrossRef Medline
64. Moscovitch M, Cabeza R, Winocur G, Nadel L (2016) Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol 67:105-134. CrossRef Medline
65. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7:217-227. CrossRef Medline
66. Neunuebel JP, Knierim JJ (2014) CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 81:416-427. CrossRef Medline
67. Nonaka A, Toyoda T, Miura Y, Hitora-Imamura N, Naka M, Eguchi M, Yamaguchi S, Ikegaya Y, Matsuki N, Nomura H (2014) Synaptic plasticity associated with a memory engram in the basolateral amygdala. J Neurosci 34:9305-9309. CrossRef Medline
68. Olds J, Milner P (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47:419-427. CrossRef Medline
69. Orbach J (1998) The neuropsychological theories of Lashley and Hebb. Lanham, MD: University Press of America.
70. Orbach J (1999) The neuropsychological theories of Lashley and Hebb. http://www.cogsci.ecs.soton.ac.uk/cgi/psyc/newpsy?10.029.
71. Park S, Kramer EE, Mercaldo V, Rashid AJ, Insel N, Frankland PW, Josselyn SA (2016) Neuronal allocation to a hippocampal engram. Neuropsychopharmacology 41:2987-2993. CrossRef Medline
72. Penfield W (1968) Engrams in the human brain: mechanisms of memory. Proc R Soc Med 61:831-840. Medline
73. Penfield W (1977) No man alone: a neurosurgeon’s life. New York: Little Brown.
74. Penfield W, Boldfrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60.
75. Penfield W, Evans J (1935) The frontal lobe in man: a clinical study of maximum removal. Brain 58:115-133. CrossRef
76. Penfield W, Milner B (1958) Memory deficit produced by bilateral lesions in the hippocampal zone. AMA Arch Neurol Psychiatry 79:475-497. CrossRef Medline
77. Penfield W, Perot P (1963) The brain’s record of auditory and visual experience:a final summary and discussion. Brain 86:595-696. CrossRef Medline
78. Poo MM, Pignatelli M, Ryan TJ, Tonegawa S, Bonhoeffer T, Martin KC, Rudenko A, Tsai LH, Tsien RW, Fishell G, Mullins C, Gonçalves JT, Shtrahman M, Johnston ST, Gage FH, Dan Y, Long J, Buzsáki G, Stevens C (2016) What is memory? The present state of the engram. BMC Biol 14:40. CrossRef Medline
79. Port RL, Romano AG, Steinmetz JE, Mikhail AA, PattersonMM (1986) Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. Behav Neurosci 100:745-752. CrossRef Medline
80. Ramirez S, Liu X, Lin PA, Suh J, Pignatelli M, Redondo RL, Ryan TJ, Tonegawa S (2013) Creating a false memory in the hippocampus. Science 341:387-391. CrossRef Medline
81. Ramirez S, Liu X, MacDonald CJ, Moffa A, Zhou J, Redondo RL, Tonegawa S (2015) Activating positive memory engrams suppresses depression-like behaviour. Nature 522:335-339. CrossRef Medline
82. Rashid AJ, Yan C, Mercaldo V, Hsiang HL, Park S, Cole CJ, De Cristofaro A, Yu J, Ramakrishnan C, Lee SY, Deisseroth K, Frankland PW, Josselyn SA (2016) Competition between engrams influences fear memory formation and recall. Science 353:383-387. CrossRef Medline
83. Redondo RL, Kim J, Arons AL, Ramirez S, Liu X, Tonegawa S (2014) Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 513:426-430. CrossRef Medline
84. RillingM (1996) The mystery of the vanished citations: James McConnell’s forgotten 1960s quest for planarian learning, a biochemical engram, and celebrity. Am Psychologist 51:589-598. CrossRef
85. Rogerson T, Jayaprakash B, Cai DJ, Sano Y, Lee YS, Zhou Y, Bekal P, Deisseroth K, Silva AJ (2016) Molecular and cellular mechanisms for trapping and activating emotional memories. PLoS One 11:e0161655. CrossRef Medline
86. Roy DS, Arons A, Mitchell TI, Pignatelli M, Ryan TJ, Tonegawa S (2016) Memory retrieval by activating engram cells in mouse models of early Alzheimer’s disease. Nature 531:508-512. CrossRef Medline
87. Rugg MD, Vilberg KL (2013) Brain networks underlying episodic memory retrieval. Curr Opin Neurobiol 23:255-260. CrossRef Medline
88. Russell B (1922) The analysis of mind. New York: Allen, Unwin.
89. Ryan TJ, Roy DS, Pignatelli M, Arons A, Tonegawa S (2015) Memory: engram cells retain memory under retrograde amnesia. Science 348:1007-1013. CrossRef Medline
90. Sakaguchi M, Hayashi Y (2012) Catching the engram: strategies to examine the memory trace. Mol Brain 5:32. CrossRef Medline
91. Schacter DL (1982) Stranger behind the engram: theories of memory and the psychology. Hillsdale, NJ: Erlbaum.
92. Schacter DL (2001) Forgotten ideas, neglected pioneers: Richard Semon and the story of memory. Abingdon, United Kingdom: Psychology.
93. Schacter DL, Eich JE, Tulving E (1978) Richard Semon’s theory of memory. J Verbal Learn Verbal Behav 17:721-743. CrossRef
94. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurochem 20:11-21. CrossRef Medline
95. Semon R (1921) The mneme. London: Allen, Unwin.
96. Semon RW (1923) Mnemic psychology. London: Allen, Unwin.
97. Shomrat T, Levin M (2013) An automated training paradigm reveals longterm memory in planarians and its persistence through head regeneration. J Exp Biol 216:3799-3810. CrossRef Medline
98. Smalheiser NR, Manev H, Costa E (2001) RNAi and brain function: was McConnell on the right track? Trends Neurosci 24:216-218. CrossRef Medline
99. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behav Neurosci 100:729-744. CrossRef Medline
100. Squire LR (1987) Memory and brain. New York: Oxford UP.
101. Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation:a neurobiological perspective. Curr Opin Neurobiol 5:169-177. CrossRef Medline
102. Steinmetz JE, Lavond DG, Ivkovich D, Logan CG, Thompson RF (1992) Disruption of classical eyelid conditioning after cerebellar lesions: damage to a memory trace system or a simple performance deficit? J Neurosci 12:4403-4426. Medline
103. Stern L (2013) Psychological hijinks. APA Monitor 44:24-25.
104. Tanaka KZ, Pevzner A, Hamidi AB, Nakazawa Y, Graham J, Wiltgen BJ (2014) Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron 84:347-354. CrossRef Medline
105. Thompson R, McConnell J (1955) Classical conditioning in the planarian, Dugesia dorotocephala. J Comp Physiol Psychol 48:65-68. CrossRef Medline
106. Thompson RF (1998) Richard F. Thompson. In: The history of neuroscience in autobiography (Squire LR, ed), pp 520-550. San Diego: Academic.
107. Tonegawa S, Liu X, Ramirez S, Redondo R (2015a) Memory engram cells have come of age. Neuron 87:918-931. CrossRef Medline
108. Tonegawa S, Pignatelli M, Roy DS, Ryan TJ (2015b) Memory engram storage and retrieval. Curr Opin Neurobiol 35:101-109. CrossRef Medline
109. Tulving E (1982) Synergistic ecphory in recall and recognition. Can J Psychol 36:130-147. CrossRef
110. Welsh JP, Harvey JA (1991) Pavlovian conditioning in the rabbit during inactivation of the interpositus nucleus. J Physiol 444:459-480. CrossRef Medline
111. Wheeler AL, Teixeira CM, Wang AH, Xiong X, Kovacevic N, Lerch JP, McIntosh AR, Parkinson J, Frankland PW (2013) Identification of a functional connectome for long-term fear memory in mice. PLoS Comput Biol 9:e1002853. CrossRef Medline
112. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679. CrossRef Medline
113. Winocur G, Moscovitch M, Bontempi B (2010) Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal-neocortical interactions. Neuropsychologia 48:2339-2356. CrossRef Medline
114. Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit: II. Lesions of the cerebellar cortex. Exp Brain Res 60:99-113. CrossRef Medline
115. Yiu AP, Mercaldo V, Yan C, Richards B, Rashid AJ, Hsiang HL, Pressey J, Mahadevan V, Tran MM, Kushner SA, Woodin MA, Frankland PW, Josselyn SA (2014) Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 83:722-735. CrossRef Medline
116. Yoshii T, Hosokawa H, Matsuo N (2016) Pharmacogenetic reactivation of the original engram evokes an extinguished fear memory. Neuropharmacology 113:1-9. CrossRef Medline