1932

Abstract

Memories for events are thought to be represented in sparse, distributed neuronal ensembles (or engrams). In this article, we review how neurons are chosen to become part of a particular engram, via a process of neuronal allocation. Experiments in rodents indicate that eligible neurons compete for allocation to a given engram, with more excitable neurons winning this competition. Moreover, fluctuations in neuronal excitability determine how engrams interact, promoting either memory integration (via coallocation to overlapping engrams) or separation (via disallocation to nonoverlapping engrams). In parallel with rodent studies, recent findings in humans verify the importance of this memory integration process for linking memories that occur close in time or share related content. A deeper understanding of allocation promises to provide insights into the logic underlying how knowledge is normally organized in the brain and the disorders in which this process has gone awry.

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2018-07-08
2024-10-03
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Literature Cited

  1. Abraham WC, Bear MF 1996. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126–30
    [Google Scholar]
  2. Alkon DL 1974. Associative training of Hermissenda. J. Gen. Physiol 64:70–84
    [Google Scholar]
  3. Alkon DL 1984a. Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037–45
    [Google Scholar]
  4. Alkon DL 1984b. Changes of membrane currents during learning. J. Exp. Biol. 112:95–112
    [Google Scholar]
  5. Alkon DL, Lederhendler I, Shoukimas JJ 1982. Primary changes of membrane currents during retention of associative learning. Science 215:693–95
    [Google Scholar]
  6. Alkon DL, Sakakibara M, Forman R, Harrigan J, Lederhendler I, Farley J 1985. Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behav. Neural Biol. 44:278–300
    [Google Scholar]
  7. Amari S-I 1989. Characteristics of sparsely encoded associative memory. Neural Netw 2:451–57
    [Google Scholar]
  8. Anderson MC 2003. Rethinking interference theory: executive control and the mechanisms of forgetting. J. Mem. Lang. 49:415–45
    [Google Scholar]
  9. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL 2007. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. PNAS 104:5163–68
    [Google Scholar]
  10. Armstrong K, Kose S, Williams L, Woolard A, Heckers S 2012. Impaired associative inference in patients with schizophrenia. Schizophr. Bull. 38:622–29
    [Google Scholar]
  11. Barco A, Alarcon JM, Kandel ER 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703
    [Google Scholar]
  12. Barco A, Pittenger C, Kandel ER 2003. CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin. Ther. Targets 7:101–14
    [Google Scholar]
  13. Barron HC, Vogels TP, Behrens TE, Ramaswami M 2017. Inhibitory engrams in perception and memory. PNAS 114:6666–74
    [Google Scholar]
  14. Barron HC, Vogels TP, Emir UE, Makin TR, O'Shea J et al. 2016. Unmasking latent inhibitory connections in human cortex to reveal dormant cortical memories. Neuron 90:191–203
    [Google Scholar]
  15. Benito E, Barco A 2010. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33:230–40
    [Google Scholar]
  16. Bergstrom HC, Johnson LR 2014. An organization of visual and auditory fear conditioning in the lateral amygdala. Neurobiol. Learn. Mem. 116:1–13
    [Google Scholar]
  17. Beyeler A, Namburi P, Glober GF, Simonnet C, Calhoon GG et al. 2016. Divergent routing of positive and negative information from the amygdala during memory retrieval. Neuron 90:348–61
    [Google Scholar]
  18. Bossert JM, Stern AL, Theberge FR, Cifani C, Koya E et al. 2011. Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat. Neurosci. 14:420–22
    [Google Scholar]
  19. Brightwell JJ, Smith CA, Neve RL, Colombo PJ 2007. Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn. Mem. 14:195–99
    [Google Scholar]
  20. Buonomano D 2011. Brain Bugs: How the Brain's Flaws Shape Our Lives New York: W. W. Norton & Co.
    [Google Scholar]
  21. Burghardt NS, Park EH, Hen R, Fenton AA 2012. Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 22:1795–808
    [Google Scholar]
  22. Cai DJ, Aharoni D, Shuman T, Shobe J, Biane J et al. 2016. A shared neural ensemble links distinct contextual memories encoded close in time. Nature 534:115–18
    [Google Scholar]
  23. Catterall WA 1984. The molecular basis of neuronal excitability. Science 223:653–61
    [Google Scholar]
  24. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL et al. 2005. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15:579–86
    [Google Scholar]
  25. Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R 2011. Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1004–15
    [Google Scholar]
  26. Cohen JD, Bolstad M, Lee AK 2017. Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments. eLife 6:e23040
    [Google Scholar]
  27. Cowansage KK, Shuman T, Dillingham BC, Chang A, Golshani P, Mayford M 2014. Direct reactivation of a coherent neocortical memory of context. Neuron 84:432–41
    [Google Scholar]
  28. Czajkowski R, Jayaprakash B, Wiltgen B, Rogerson T, Guzman-Karlsson MC et al. 2014. Encoding and storage of spatial information in the retrosplenial cortex. PNAS 111:8661–66
    [Google Scholar]
  29. Das T, Ivleva EI, Wagner AD, Stark CE, Tamminga CA 2014. Loss of pattern separation performance in schizophrenia suggests dentate gyrus dysfunction. Schizophr. Res. 159:193–97
    [Google Scholar]
  30. Davis M 1992. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15:353–75
    [Google Scholar]
  31. Denny CA, Kheirbek MA, Alba EL, Tanaka KF, Brachman RA et al. 2014. Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron 83:189–201
    [Google Scholar]
  32. Disterhoft JF, Coulter DA, Alkon DL 1986. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. PNAS 83:2733–37
    [Google Scholar]
  33. Dong Y, Green T, Saal D, Marie H, Neve R et al. 2006. CREB modulates excitability of nucleus accumbens neurons. Nat. Neurosci. 9:475–77
    [Google Scholar]
  34. Drew LJ, Kheirbek MA, Luna VM, Denny CA, Cloidt MA et al. 2016. Activation of local inhibitory circuits in the dentate gyrus by adult-born neurons. Hippocampus 26:763–78
    [Google Scholar]
  35. Dudai Y 2007. Memory. Science of Memory: Concepts HLI Roediger, Y Dudai, SM Fitzpatrick 13–16 New York: Oxford University Press
    [Google Scholar]
  36. Edelson M, Sharot T, Dolan RJ, Dudai Y 2011. Following the crowd: brain substrates of long-term memory conformity. Science 333:108–11
    [Google Scholar]
  37. Eichenbaum H 2000. Hippocampus: mapping or memory. Curr. Biol. 10:R785–87
    [Google Scholar]
  38. Enwright JF, Sanapala S, Foglio A, Berry R, Fish KN, Lewis DA 2016. Reduced labeling of parvalbumin neurons and perineuronal nets in the dorsolateral prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology 41:2206–14
    [Google Scholar]
  39. Epsztein J, Brecht M, Lee AK 2011. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70:109–20
    [Google Scholar]
  40. Estes WK 1955. Statistical theory of distributional phenomena in learning. Psychol. Rev. 62:369–77
    [Google Scholar]
  41. Fanselow MS, Gale GD 2003. The amygdala, fear, and memory. Ann. N. Y. Acad. Sci. 985:125–34
    [Google Scholar]
  42. Feng F, Samarth P, Pare D, Nair SS 2016. Mechanisms underlying the formation of the amygdalar fear memory trace: a computational perspective. Neuroscience 322:370–76
    [Google Scholar]
  43. Frankland PW, Josselyn SA 2015. Memory allocation. Neuropsychopharmacology 40:243
    [Google Scholar]
  44. Garner AR, Rowland DC, Hwang SY, Baumgaertel K, Roth BL et al. 2012. Generation of a synthetic memory trace. Science 335:1513–16
    [Google Scholar]
  45. Gilbert PE, Kesner RP, DeCoteau WE 1998. Memory for spatial location: role of the hippocampus in mediating spatial pattern separation. J. Neurosci. 18:804–10
    [Google Scholar]
  46. Gilboa A, Marlatte H 2017. Neurobiology of schemas and schema-mediated memory. Trends Cogn. Sci. 21:618–31
    [Google Scholar]
  47. Goosens KA, Maren S 2001. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem. 8:148–55
    [Google Scholar]
  48. Gouty-Colomer LA, Hosseini B, Marcelo IM, Schreiber J, Slump DE et al. 2015. Arc expression identifies the lateral amygdala fear memory trace. Mol. Psychiatry 21:364–75
    [Google Scholar]
  49. Guzowski JF, McNaughton BL, Barnes CA, Worley PF 1999. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 2:1120–24
    [Google Scholar]
  50. Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A et al. 2007. Neuronal competition and selection during memory formation. Science 316:457–60
    [Google Scholar]
  51. Han JH, Kushner SA, Yiu AP, Hsiang HL, Buch T et al. 2009. Selective erasure of a fear memory. Science 323:1492–96
    [Google Scholar]
  52. Hennequin G, Agnes EJ, Vogels TP 2017. Inhibitory plasticity: balance, control, and codependence. Annu. Rev. Neurosci. 40:557–79
    [Google Scholar]
  53. Howard MW, Eichenbaum H 2013. The hippocampus, time, and memory across scales. J. Exp. Psychol. Gen. 142:1211–30
    [Google Scholar]
  54. Hsiang HL, Epp JR, van den Oever MC, Yan C, Rashid AJ et al. 2014. Manipulating a “cocaine engram” in mice. J. Neurosci. 34:14115–27
    [Google Scholar]
  55. Hunsaker MR, Kesner RP 2013. The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci. Biobehav. Rev. 37:36–58
    [Google Scholar]
  56. Josselyn SA 2010. Continuing the search for the engram: examining the mechanism of fear memories. J. Psychiatry Neurosci. 35:221–28
    [Google Scholar]
  57. Josselyn SA, Kohler S, Frankland PW 2015. Finding the engram. Nat. Rev. Neurosci. 16:521–34
    [Google Scholar]
  58. Josselyn SA, Kohler S, Frankland PW 2017. Heroes of the engram. J. Neurosci. 37:4647–57
    [Google Scholar]
  59. Josselyn SA, Shi C, Carlezon WA Jr., Neve RL, Nestler EJ, Davis M 2001. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci. 21:2404–12
    [Google Scholar]
  60. Kahana MJ, Howard MW, Zaromb F, Wingfield A 2002. Age dissociates recency and lag recency effects in free recall. J. Exp. Psychol. Learn. Mem. Cogn. 28:530–40
    [Google Scholar]
  61. Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N et al. 2009. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. PNAS 106:316–21
    [Google Scholar]
  62. Kim D, Pare D, Nair SS 2013. Assignment of model amygdala neurons to the fear memory trace depends on competitive synaptic interactions. J. Neurosci. 33:14354–58
    [Google Scholar]
  63. Kim D, Samarth P, Feng F, Pare D, Nair SS 2016. Synaptic competition in the lateral amygdala and the stimulus specificity of conditioned fear: a biophysical modeling study. Brain Struct. Funct. 221:2163–82
    [Google Scholar]
  64. Kim J, Kwon JT, Kim HS, Josselyn SA, Han JH 2014. Memory recall and modifications by activating neurons with elevated CREB. Nat. Neurosci. 17:65–72
    [Google Scholar]
  65. Kim J, Pignatelli M, Xu S, Itohara S, Tonegawa S 2016. Antagonistic negative and positive neurons of the basolateral amygdala. Nat. Neurosci. 19:1636–46
    [Google Scholar]
  66. Kim J, Zhang X, Muralidhar S, LeBlanc SA, Tonegawa S 2017. Basolateral to central amygdala neural circuits for appetitive behaviors. Neuron 93:1464–79
    [Google Scholar]
  67. 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
    [Google Scholar]
  68. Kirwan CB, Stark CE 2007. Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe. Learn. Mem. 14:625–33
    [Google Scholar]
  69. Koya E, Golden SA, Harvey BK, Guez-Barber DH, Berkow A et al. 2009. Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat. Neurosci. 12:1069–73
    [Google Scholar]
  70. Kriegeskorte N, Mur M, Bandettini P 2008. Representational similarity analysis—connecting the branches of systems neuroscience. Front. Syst. Neurosci. 2:4
    [Google Scholar]
  71. Lanuza E, Moncho-Bogani J, Ledoux JE 2008. Unconditioned stimulus pathways to the amygdala: effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala. Neuroscience 155:959–68
    [Google Scholar]
  72. LeDoux JE 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23:155–84
    [Google Scholar]
  73. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM 1990. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci. 10:1062–69
    [Google Scholar]
  74. LeDoux JE, Ruggiero DA, Reis DJ 1985. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J. Comp. Neurol. 242:182–213
    [Google Scholar]
  75. Lee D, Lin BJ, Lee AK 2012. Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science 337:849–53
    [Google Scholar]
  76. Leutgeb JK, Leutgeb S, Moser MB, Moser EI 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–66
    [Google Scholar]
  77. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–98
    [Google Scholar]
  78. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J 2002. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416:90–94
    [Google Scholar]
  79. Levy BJ, Wagner AD 2013. Measuring memory reactivation with functional MRI: implications for psychological theory. Perspect. Psychol. Sci. 8:72–78
    [Google Scholar]
  80. Lewis DA, Curley AA, Glausier JR, Volk DW 2012. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 35:57–67
    [Google Scholar]
  81. Linke R, Braune G, Schwegler H 2000. Differential projection of the posterior paralaminar thalamic nuclei to the amygdaloid complex in the rat. Exp. Brain Res. 134:520–32
    [Google Scholar]
  82. Liu X, Ramirez S, Pang PT, Puryear CB, Govindarajan A et al. 2012. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484:381–85
    [Google Scholar]
  83. Loftus EF 2005. Planting misinformation in the human mind: a 30-year investigation of the malleability of memory. Learn. Mem. 12:361–66
    [Google Scholar]
  84. Lonze BE, Ginty DD 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–23
    [Google Scholar]
  85. Lucas EK, Jegarl AM, Morishita H, Clem RL 2016. Multimodal and site-specific plasticity of amygdala parvalbumin interneurons after fear learning. Neuron 91:629–43
    [Google Scholar]
  86. Mack ML, Love BC, Preston AR 2017. Building concepts one episode at a time: the hippocampus and concept formation. Neurosci. Lett. In press
    [Google Scholar]
  87. Marie H, Morishita W, Yu X, Calakos N, Malenka RC 2005. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741–52
    [Google Scholar]
  88. Marr D 1971. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. B 262:23–81
    [Google Scholar]
  89. McDonald AJ 1998. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55:257–332
    [Google Scholar]
  90. McKenzie S, Eichenbaum H 2011. Consolidation and reconsolidation: two lives of memories. Neuron 71:224–33
    [Google Scholar]
  91. McNaughton BL, Morris RGM 1987. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–15
    [Google Scholar]
  92. Milner B, Squire LR, Kandel ER 1998. Cognitive neuroscience and the study of memory. Neuron 20:445–68
    [Google Scholar]
  93. Moncada D, Viola H 2006. Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity. Neurobiol. Learn. Mem. 86:9–18
    [Google Scholar]
  94. Moncada D, Viola H 2007. Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J. Neurosci. 27:7476–81
    [Google Scholar]
  95. Morris RG, Garrud P, Rawlins JN, O'Keefe J 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681–83
    [Google Scholar]
  96. Morrison DJ, Rashid AJ, Yiu AP, Yan C, Frankland PW, Josselyn SA 2016. Parvalbumin interneurons constrain the size of the lateral amygdala engram. Neurobiol. Learn. Mem. 135:91–99
    [Google Scholar]
  97. Moyer JR Jr., Thompson LT, Disterhoft JF 1996. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 16:5536–46
    [Google Scholar]
  98. Mozzachiodi R, Byrne JH 2010. More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory. Trends Neurosci 33:17–26
    [Google Scholar]
  99. Namburi P, Beyeler A, Yorozu S, Calhoon GG, Halbert SA et al. 2015. A circuit mechanism for differentiating positive and negative associations. Nature 520:675–78
    [Google Scholar]
  100. Norman KA, O'Reilly RC 2003. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol. Rev. 110:611–46
    [Google Scholar]
  101. Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF 2003. Watermaze learning enhances excitability of CA1 pyramidal neurons. J. Neurophysiol. 90:2171–79
    [Google Scholar]
  102. O'Keefe J, Dostrovsky J 1971. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–75
    [Google Scholar]
  103. Pape HC, Pare D 2010. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 90:419–63
    [Google Scholar]
  104. Park S, Kramer EE, Mercaldo V, Rashid AJ, Insel N et al. 2016. Neuronal allocation to a hippocampal engram. Neuropsychopharmacology 41:2987–93
    [Google Scholar]
  105. Parsons RG, Davis M 2012. A metaplasticity-like mechanism supports the selection of fear memories: role of protein kinase A in the amygdala. J. Neurosci. 32:7843–51
    [Google Scholar]
  106. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D 2005. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat. Neurosci. 8:51–60
    [Google Scholar]
  107. Quirk GJ, Armony JL, LeDoux JE 1997. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19:613–24
    [Google Scholar]
  108. Quirk GJ, Repa C, LeDoux JE 1995. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15:1029–39
    [Google Scholar]
  109. Ramirez S, Liu X, Lin PA, Suh J, Pignatelli M et al. 2013. Creating a false memory in the hippocampus. Science 341:387–91
    [Google Scholar]
  110. Rashid AJ, Yan C, Mercaldo V, Hsiang HL, Park S et al. 2016. Competition between engrams influences fear memory formation and recall. Science 353:383–87
    [Google Scholar]
  111. 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 513:426–30
    [Google Scholar]
  112. Reijmers LG, Perkins BL, Matsuo N, Mayford M 2007. Localization of a stable neural correlate of associative memory. Science 317:1230–33
    [Google Scholar]
  113. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE 2001. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat. Neurosci. 4:724–31
    [Google Scholar]
  114. Rexach JE, Clark PM, Mason DE, Neve RL, Peters EC, Hsieh-Wilson LC 2012. Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation. Nat. Chem. Biol. 8:253–61
    [Google Scholar]
  115. Rich PD, Liaw HP, Lee AK 2014. Place cells: Large environments reveal the statistical structure governing hippocampal representations. Science 345:814–17
    [Google Scholar]
  116. Rickgauer JP, Deisseroth K, Tank DW 2014. Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields. Nat. Neurosci. 17:1816–24
    [Google Scholar]
  117. Rogerson T, Cai DJ, Frank A, Sano Y, Shobe J et al. 2014. Synaptic tagging during memory allocation. Nat. Rev. Neurosci. 15:157–69
    [Google Scholar]
  118. Rogerson T, Jayaprakash B, Cai DJ, Sano Y, Lee YS et al. 2016. Molecular and cellular mechanisms for trapping and activating emotional memories. PLOS ONE 11:e0161655
    [Google Scholar]
  119. Rolls ET, Treves A 1990. The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain. Network 1:407–21
    [Google Scholar]
  120. Rolls ET, Treves A 1994. Neural networks in the brain involved in memory and recall. Prog. Brain Res. 102:335–41
    [Google Scholar]
  121. Rumelhart DE, Zipser D 1985. Feature discovery by competitive learning. Cogn. Sci. 9:75–112
    [Google Scholar]
  122. Rumpel S, LeDoux J, Zador A, Malinow R 2005. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88
    [Google Scholar]
  123. Sano Y, Shobe JL, Zhou M, Huang S, Shuman T et al. 2014. CREB regulates memory allocation in the insular cortex. Curr. Biol. 24:2833–37
    [Google Scholar]
  124. Sargin D, Mercaldo V, Yiu AP, Higgs G, Han JH et al. 2013. CREB regulates spine density of lateral amygdala neurons: implications for memory allocation. Front. Behav. Neurosci. 7:209
    [Google Scholar]
  125. Schacter DL 2001. Forgotten Ideas, Neglected Pioneers: Richard Semon and the Story of Memory Hove, UK: Psychol. Press
    [Google Scholar]
  126. Schacter DL, Guerin SA, St Jacques PL 2011. Memory distortion: an adaptive perspective. Trends Cogn. Sci. 15:467–74
    [Google Scholar]
  127. Schlichting ML, Frankland PW 2017. Memory allocation and integration in rodents and humans. Curr. Opin. Behav. Sci. 17:90–98
    [Google Scholar]
  128. Schlichting ML, Preston AR 2015. Memory integration: neural mechanisms and implications for behavior. Curr. Opin. Behav. Sci. 1:1–8
    [Google Scholar]
  129. Schlichting ML, Zeithamova D, Preston AR 2014. CA1 subfield contributions to memory integration and inference. Hippocampus 24:1248–60
    [Google Scholar]
  130. Scholz KP, Byrne JH 1987. Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235:685–87
    [Google Scholar]
  131. Schroeder BC, Kubisch C, Stein V, Jentsch TJ 1998. Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature 396:687–90
    [Google Scholar]
  132. Scoville WB, Milner B 1957. Loss of recent memory after bilateral hippocampal lesions. J. Neurochem. 20:11–21
    [Google Scholar]
  133. Sehgal M, Song C, Ehlers VL, Moyer JR Jr 2013. Learning to learn—intrinsic plasticity as a metaplasticity mechanism for memory formation. Neurobiol. Learn. Mem. 105:186–99
    [Google Scholar]
  134. Sekeres MJ, Mercaldo V, Richards B, Sargin D, Mahadevan V et al. 2012. Increasing CRTC1 function in the dentate gyrus during memory formation or reactivation increases memory strength without compromising memory quality. J. Neurosci. 32:17857–68
    [Google Scholar]
  135. Sekeres MJ, Neve RL, Frankland PW, Josselyn SA 2010. Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. Learn. Mem. 17:280–83
    [Google Scholar]
  136. Semon RW 1921. The Mneme London: G. Allen & Unwin304 pp
    [Google Scholar]
  137. Shi C, Davis M 1999. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J. Neurosci. 19:420–30
    [Google Scholar]
  138. Shohamy D, Wagner AD 2008. Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events. Neuron 60:378–89
    [Google Scholar]
  139. Silva AJ, Zhou Y, Rogerson T, Shobe J, Balaji J 2009. Molecular and cellular approaches to memory allocation in neural circuits. Science 326:391–95
    [Google Scholar]
  140. Song C, Detert JA, Sehgal M, Moyer JR Jr 2012. Trace fear conditioning enhances synaptic and intrinsic plasticity in rat hippocampus. J. Neurophysiol. 107:3397–408
    [Google Scholar]
  141. Squire LR 1992. Declarative and nondeclarative memory: multiple brain systems supporting learning and memory. J. Cogn. Neurosci. 4:232–43
    [Google Scholar]
  142. Stefanelli T, Bertollini C, Luscher C, Muller D, Mendez P 2016. Hippocampal somatostatin interneurons control the size of neuronal memory ensembles. Neuron 89:1074–85
    [Google Scholar]
  143. Storm BC, Jobe TA 2012. Retrieval-induced forgetting predicts failure to recall negative autobiographical memories. Psychol. Sci. 23:1356–63
    [Google Scholar]
  144. Tanaka KZ, Pevzner A, Hamidi AB, Nakazawa Y, Graham J, Wiltgen BJ 2014. Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron 84:347–54
    [Google Scholar]
  145. Tayler KK, Tanaka KZ, Reijmers LG, Wiltgen BJ 2013. Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr. Biol. 23:99–106
    [Google Scholar]
  146. Thome A, Marrone DF, Ellmore TM, Chawla MK, Lipa P et al. 2017. Evidence for an evolutionarily conserved memory coding scheme in the mammalian hippocampus. J. Neurosci. 37:2795–801
    [Google Scholar]
  147. Thompson LT, Moyer JR Jr., Disterhoft JF 1996. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J. Neurophysiol. 76:1836–49
    [Google Scholar]
  148. Titley HK, Brunel N, Hansel C 2017. Toward a neurocentric view of learning. Neuron 95:19–32
    [Google Scholar]
  149. Tonegawa S, Liu X, Ramirez S, Redondo R 2015. Memory engram cells have come of age. Neuron 87:918–31
    [Google Scholar]
  150. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA et al. 2007. Schemas and memory consolidation. Science 316:76–82
    [Google Scholar]
  151. Turrigiano G 2011. Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 34:89–103
    [Google Scholar]
  152. Vazdarjanova A, Ramirez-Amaya V, Insel N, Plummer TK, Rosi S et al. 2006. Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J. Comp. Neurol. 498:317–29
    [Google Scholar]
  153. Viola H, Ballarini F, Martinez MC, Moncada D 2014. The tagging and capture hypothesis from synapse to memory. Prog. Mol. Biol. Transl. Sci. 122:391–423
    [Google Scholar]
  154. Viosca J, Malleret G, Bourtchouladze R, Benito E, Vronskava S et al. 2009. Chronic enhancement of CREB activity in the hippocampus interferes with the retrieval of spatial information. Learn. Mem. 16:198–209
    [Google Scholar]
  155. Wallace DL, Han MH, Graham DL, Green TA, Vialou V et al. 2009. CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat. Neurosci. 12:200–9
    [Google Scholar]
  156. Wallace TL, Stellitano KE, Neve RL, Duman RS 2004. Effects of cyclic adenosine monophosphate response element binding protein overexpression in the basolateral amygdala on behavioral models of depression and anxiety. Biol. Psychiatry 56:151–60
    [Google Scholar]
  157. White NM, Packard MG, McDonald RJ 2013. Dissociation of memory systems: The story unfolds. Behav. Neurosci. 127:813–34
    [Google Scholar]
  158. Wilson MA, McNaughton BL 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055–58
    [Google Scholar]
  159. Wimber M, Alink A, Charest I, Kriegeskorte N, Anderson MC 2015. Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression. Nat. Neurosci. 18:582–89
    [Google Scholar]
  160. Wolfe J, Houweling AR, Brecht M 2010. Sparse and powerful cortical spikes. Curr. Opin. Neurobiol. 20:306–12
    [Google Scholar]
  161. Woody CD, Black-Cleworth P 1973. Differences in excitability of cortical neurons as a function of motor projection in conditioned cats. J. Neurophysiol. 36:1104–16
    [Google Scholar]
  162. Yang Y, Liu DQ, Huang W, Deng J, Sun Y et al. 2016. Selective synaptic remodeling of amygdalocortical connections associated with fear memory. Nat. Neurosci. 19:1348–55
    [Google Scholar]
  163. Yassa MA, Stark CE 2011. Pattern separation in the hippocampus. Trends Neurosci 34:515–25
    [Google Scholar]
  164. Yiu AP, Mercaldo V, Yan C, Richards B, Rashid AJ et al. 2014. Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 83:722–35
    [Google Scholar]
  165. Yokose J, Okubo-Suzuki R, Nomoto M, Ohkawa N, Nishizono H et al. 2017. Overlapping memory trace indispensable for linking, but not recalling, individual memories. Science 355:398–403
    [Google Scholar]
  166. Zeithamova D, Preston AR 2017. Temporal proximity promotes integration of overlapping events. J. Cogn. Neurosci. 29:1311–23
    [Google Scholar]
  167. Zeithamova D, Schlichting ML, Preston AR 2012. The hippocampus and inferential reasoning: building memories to navigate future decisions. Front. Hum. Neurosci. 6:70
    [Google Scholar]
  168. Zhang W, Linden DJ 2003. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 4:885–900
    [Google Scholar]
  169. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T et al. 2009. CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat. Neurosci. 12:1438–43
    [Google Scholar]
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