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Cortico-Hippocampal Circuits for Memory Consolidation: The Role of the Prefrontal Cortex

  • Lisa Genzel
  • Francesco P. Battaglia
Chapter
Part of the Studies in Neuroscience, Psychology and Behavioral Economics book series (SNPBE)

Abstract

Memory is made up of multiple interacting systems, intervening at different times during the lifetime of the memory, and organizing information in different ways. One system is centered on the hippocampus and it is key for episodic memory and initial memory acquisition; while another system is based in the neocortex and is involved in storage of remote memories and semantic memory. These two stores communicate during sleep and other quiet periods, when neural patterns related to previously acquired memories are replayed. This reactivation is thought to engage plasticity processes in many brain areas, therefore enabling memory consolidation. We review here some of the experimental evidence on memory replay and dynamical interactions between cortex and hippocampus during sleep, with a focus on the prefrontal cortex, one of the key cortical areas for memory.

Keyword

Hippocampus Prefrontal cortex Schema Memory Consolidation System Sleep 

References

  1. Amit DJ (1989) Modeling brain function. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  2. Andrillon T, Nir Y et al (2011) Sleep spindles in humans: insights from intracranial EEG and unit recordings. J Neurosci 31(49):17821–17834PubMedPubMedCentralCrossRefGoogle Scholar
  3. Battaglia FP, Sutherland GR et al (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state†transitions. Learn Mem 11(6):697–704PubMedPubMedCentralCrossRefGoogle Scholar
  4. Battaglia FP, Benchenane K et al (2011) The hippocampus: hub of brain network communication for memory. Trends Cogn Sci 15(7):310–318PubMedGoogle Scholar
  5. Battaglia FP, Borensztajn G et al (2012) Structured cognition and neural systems: from rats to language. Neurosci Biobehav Rev 36(7):1626–1639PubMedCrossRefGoogle Scholar
  6. Bayley PJ, Gold JJ et al (2005) The neuroanatomy of remote memory. Neuron 46(5):799–810PubMedPubMedCentralCrossRefGoogle Scholar
  7. Benchenane K, Peyrache A et al (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66(6):921–936PubMedCrossRefGoogle Scholar
  8. Benchenane K, Tiesinga PH et al (2011) Oscillations in the prefrontal cortex: a gateway to memory and attention. Curr Opin Neurobiol 21:475–485PubMedCrossRefGoogle Scholar
  9. Bethus I, Tse D et al (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30(5):1610–1618PubMedCrossRefGoogle Scholar
  10. Buzsaki G (1989) Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31(3):551–570PubMedCrossRefGoogle Scholar
  11. Buzsaki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25(10):1073–1188PubMedPubMedCentralCrossRefGoogle Scholar
  12. Buzsáki G, Horváth Z et al (1992) High-frequency network oscillation in the hippocampus. Science 256(5059):1025–1027PubMedCrossRefGoogle Scholar
  13. Carr MF, Jadhav SP et al (2011) Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci 14(2):147–153PubMedPubMedCentralCrossRefGoogle Scholar
  14. Carr MF, Karlsson MP, Frank LM (2012) Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 23; 75(4):700–713Google Scholar
  15. Cheng J, Ji D (2013) Rigid firing sequences undermine spatial memory codes in a neurodegenerative mouse model. Elife 2:e00647PubMedPubMedCentralCrossRefGoogle Scholar
  16. Clemens Z, Fabó DN et al (2005) Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132:529–535PubMedCrossRefGoogle Scholar
  17. Clemens Z, Fabó DN et al (2006) Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci Lett 403:52–56PubMedCrossRefGoogle Scholar
  18. Clemens Z, Mölle M et al (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130(11):2868–2878PubMedCrossRefGoogle Scholar
  19. Clemens Z, Mölle M et al (2011) Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci 33(3):511–520PubMedCrossRefGoogle Scholar
  20. Cowansage KK, Shuman T et al (2014) Direct reactivation of a coherent neocortical memory of context. Neuron 84(2):432–441PubMedPubMedCentralCrossRefGoogle Scholar
  21. Davidson TJ, Kloosterman F et al (2009) Hippocampal replay of extended experience. Neuron 63(4):497–507PubMedPubMedCentralCrossRefGoogle Scholar
  22. de Lavilleon G, Lacroix MM et al (2015) Explicit memory creation during sleep demonstrates a causal role of place cells in navigation. Nat Neurosci 18(4):493–495PubMedCrossRefGoogle Scholar
  23. Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10(10):1241–1242PubMedPubMedCentralCrossRefGoogle Scholar
  24. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126PubMedGoogle Scholar
  25. Dragoi G, Tonegawa S (2011) Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469(7330):397–401PubMedCrossRefGoogle Scholar
  26. Dragoi G, Tonegawa S (2013) Development of schemas revealed by prior experience and NMDA receptor knock-out. Elife 2:e01326PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dresler M, Genzel L et al (2010a) Off-line memory consolidation impairments in multiple sclerosis patients receiving high-dose corticosteroid treatment mirror consolidation impairments in depression. Psychoneuroendocrinology 35(8):1194–1202PubMedCrossRefGoogle Scholar
  28. Dresler M, Kluge M et al (2010b) Impaired off-line memory consolidation in depression. Eur Neuropsychopharmacol 20:553–561PubMedCrossRefGoogle Scholar
  29. Dresler M, Kluge M et al (2011) A double dissociation of memory impairments in major depression. J Psychiatr Res 45(12):1593–1599PubMedCrossRefGoogle Scholar
  30. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20(1):1–10PubMedPubMedCentralGoogle Scholar
  31. Ekstrom AD, Meltzer J et al (2001) NMDA receptor antagonism blocks experience-dependent expansion of hippocampal “place fields”. Neuron 31(4):631–638PubMedCrossRefGoogle Scholar
  32. Euston DR, Tatsuno M et al (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318(5853):1147–1150PubMedCrossRefGoogle Scholar
  33. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440(7084):680–683PubMedCrossRefGoogle Scholar
  34. Gais S, Helms K et al (2002) Increased density of sleep spindles after extensive learning of a declarative memory task. J Sleep Res 11(Suppl 1):147Google Scholar
  35. Gardner RJ, Kersante F et al (2014) Neural oscillations during non-rapid eye movement sleep as biomarkers of circuit dysfunction in schizophrenia. Eur J Neurosci 39(7):1091–1106PubMedCrossRefGoogle Scholar
  36. Genzel L, Robertson EM (2015) To replay, perchance to consolidate. PLoS Biol 13(10):e1002285PubMedPubMedCentralCrossRefGoogle Scholar
  37. Genzel L, Dresler M et al (2009) Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep 32(3):302–310PubMedPubMedCentralGoogle Scholar
  38. Genzel L, Ali E et al (2011) Sleep-dependent memory consolidation of a new task is inhibited in psychiatric patients. J Psychiatr Res 45(4):555–560PubMedCrossRefGoogle Scholar
  39. Genzel L, Kiefer T et al (2012) Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology 37(7):987–989PubMedCrossRefGoogle Scholar
  40. Genzel L, Kroes MCW et al (2014) Light sleep vs. slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci 37(1):10–19PubMedCrossRefGoogle Scholar
  41. Genzel L, Dresler M et al (2015a) Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol Psychiatry 77(2):177–186PubMedCrossRefGoogle Scholar
  42. Genzel L, Spoormaker VI et al (2015b) The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol Learn Mem 122:110–121PubMedCrossRefGoogle Scholar
  43. Ghosh VE, Gilboa A (2014) What is a memory schema? A historical perspective on current neuroscience literature. Neuropsychologia 53:104–114PubMedCrossRefGoogle Scholar
  44. Girardeau G, Benchenane K et al (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222–1223PubMedCrossRefGoogle Scholar
  45. Godsil BP, Kiss JP et al (2013) The hippocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur Neuropsychopharmacol 23(10):1165–1181PubMedCrossRefGoogle Scholar
  46. Gupta AS, van der Meer MAA et al. (2012) Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15(7):1032–1039Google Scholar
  47. Hahn TTG, Sakmann B et al (2006) Phase-locking of hippocampal interneurons’ membrane potential to neocortical up-down states. Nat Neurosci 9(11):1359–1361PubMedCrossRefGoogle Scholar
  48. Herry C, Johansen JP (2014) Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci 17(12):1644–1654PubMedCrossRefGoogle Scholar
  49. Hoffman KL, McNaughton BL (2002) Coordinated reactivation of distributed memory traces in primate neocortex. Science 297(5589):2070–2073PubMedCrossRefGoogle Scholar
  50. Isomura Y, Sirota A et al (2006) Integration and segregation of activity in Entorhinal-Hippocampal subregions by neocortical slow oscillations. Neuron 52(5):871–882PubMedCrossRefGoogle Scholar
  51. Ito HT, Zhang S-J et al (2015) A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation. Nature 522(7554):50–55PubMedCrossRefGoogle Scholar
  52. Jadhav SP, Kemere C et al. (2012) “Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory.” Science 336(6087):1454–1458Google Scholar
  53. Jadhav SP, Rothschild G et al (2016) Coordinated excitation and inhibition of prefrontal ensembles during awake hippocampal sharp-wave ripple events. Neuron 90(1):113–127PubMedCrossRefGoogle Scholar
  54. Johnson A, Redish AD (2007) Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27(45):12176–12189PubMedCrossRefGoogle Scholar
  55. Kao CY, Stalla G et al (2015) Norepinephrine and corticosterone in the medial prefrontal cortex and hippocampus predict PTSD-like symptoms in mice. Eur J Neurosci 41(9):1139–1148PubMedCrossRefGoogle Scholar
  56. Kaplan R, Adhikari MH et al (2016) Hippocampal sharp-wave ripples influence selective activation of the default mode network. Curr Biol 26(5):686–691PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kentros C, Hargreaves E et al (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280(5372):2121–2126PubMedCrossRefGoogle Scholar
  58. Kudrimoti HS, Barnes CA et al (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19(10):4090–4101PubMedGoogle Scholar
  59. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36(6):1183–1194PubMedCrossRefGoogle Scholar
  60. Lesburgueres E, Gobbo OL et al (2011) Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331(6019):924–928PubMedCrossRefGoogle Scholar
  61. Lewis PA, Durrant SJ (2011) Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn Sci 15(8):343–351PubMedCrossRefGoogle Scholar
  62. Logothetis NK, Eschenko O et al (2012) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491(7425):547–553PubMedCrossRefGoogle Scholar
  63. Luczak A, Barthó P et al (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A 104(1):347–352PubMedCrossRefGoogle Scholar
  64. Maingret N, Girardeau G et al (2016) “Hippocampo-cortical coupling mediates memory consolidation during sleep”. Nat Neurosci (in press)Google Scholar
  65. Manoach DS, Cain MS et al (2004) A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biol Psychiatry 56:951–956PubMedCrossRefGoogle Scholar
  66. Manoach DS, Thakkar KN et al (2010) Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J Psychiatr Res 44(2):112–120PubMedCrossRefGoogle Scholar
  67. Marr D (1970) A theory for cerebral neocortex. Proc Roy Soc Lond Ser B Biol Sci 176:161–234CrossRefGoogle Scholar
  68. Marr D (1971) A theory for archicortex. Philos Trans Roy Soc Lond Ser B Biol Sci 262:23–81CrossRefGoogle Scholar
  69. McClelland JL, McNaughton BL et al (1995) Why there are complementary learning systems in the hippocampus and neocortex: Insights form the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419–457PubMedCrossRefGoogle Scholar
  70. McNamara CG, Tejero-Cantero A et al (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17(12):1658–1660PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mölle M, Eschenko O et al (2009) The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur J Neurosci 29(5):1071–1081PubMedCrossRefGoogle Scholar
  72. Mongillo G, Barak O et al (2008) Synaptic theory of working memory. Science 319(5869):1543–1546PubMedCrossRefGoogle Scholar
  73. Moscovitch M, Cabeza R et al (2016) Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol 67:105–134PubMedPubMedCentralCrossRefGoogle Scholar
  74. Nieuwenhuis ILC, Takashima A (2011) The role of the ventromedial prefrontal cortex in memory consolidation. Behav Brain Res 218(2):325–334PubMedCrossRefGoogle Scholar
  75. Nir Y, Staba Richard J et al (2011) Regional slow waves and spindles in human sleep. Neuron 70(1):153–169PubMedPubMedCentralCrossRefGoogle Scholar
  76. Novitskaya Y, Sara SJ et al (2016) Ripple-triggered stimulation of the locus coeruleus during post-learning sleep disrupts ripple/spindle coupling and impairs memory consolidation. Learn Mem 23(5):238–248PubMedCrossRefGoogle Scholar
  77. O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51(1):78–109PubMedCrossRefGoogle Scholar
  78. O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3(3):317–330PubMedCrossRefGoogle Scholar
  79. Peyrache A, Khamassi M et al (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12(7):919–926PubMedCrossRefGoogle Scholar
  80. Peyrache A, Battaglia FP et al (2011) Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci 108(41):17207–17212PubMedPubMedCentralCrossRefGoogle Scholar
  81. Peyrache A, Lacroix MM et al (2015) Internally organized mechanisms of the head direction sense. Nat Neurosci 18(4):569–575PubMedPubMedCentralCrossRefGoogle Scholar
  82. Pfeiffer BE, Foster DJ (2013) Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497(7447):74–79PubMedPubMedCentralCrossRefGoogle Scholar
  83. Phillips K-G, Bartsch U et al (2012) Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76(3):526–533PubMedPubMedCentralCrossRefGoogle Scholar
  84. Plenz D, Thiagarajan TC (2007) The organizing principles of neuronal avalanches: cell assemblies in the cortex? Trends Neurosci 30(3):101–110PubMedCrossRefGoogle Scholar
  85. Polta SA, Fenzl T et al (2013) Prognostic and symptomatic aspects of rapid eye movement sleep in a mouse model of posttraumatic stress disorder. Front Behav Neurosci 7:60PubMedPubMedCentralCrossRefGoogle Scholar
  86. Preston AR, Eichenbaum H (2013) Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 23(17):R764–773PubMedPubMedCentralCrossRefGoogle Scholar
  87. Rajasethupathy P, Sankaran S et al (2015) Projections from neocortex mediate top-down control of memory retrieval. Nature 526(7575):653–659PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ramanathan DS, Gulati T et al (2015) Sleep-dependent reactivation of ensembles in motor cortex promotes skill consolidation. PLoS Biol 13(9):e1002263PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ramirez-Villegas JF, Logothetis NK et al (2015) Diversity of sharp-wave-ripple LFP signatures reveals differentiated brain-wide dynamical events. Proc Natl Acad Sci U S A 112(46):E6379–6387PubMedPubMedCentralCrossRefGoogle Scholar
  90. Redish AD (2016) Vicarious trial and error. Nat Rev Neurosci 17(3):147–159PubMedCrossRefGoogle Scholar
  91. Reichinnek S, Kuensting T et al (2010) Field potential signature of distinct multicellular activity patterns in the mouse hippocampus. J Neurosci 30(46):15441–15449PubMedCrossRefGoogle Scholar
  92. Sadowski JH, Jones MW et al (2016) Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. Cell Rep 14(8):1916–1929PubMedPubMedCentralCrossRefGoogle Scholar
  93. Schacter DL, Addis DR et al (2012) The future of memory: remembering, imagining, and the brain. Neuron 76(4):677–694PubMedCrossRefGoogle Scholar
  94. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21(5):1123–1128PubMedCrossRefGoogle Scholar
  95. Siapas AG, Lubenov EV et al (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46(1):141–151PubMedCrossRefGoogle Scholar
  96. Silva D, Feng T et al (2015) Trajectory events across hippocampal place cells require previous experience. Nat Neurosci 18(12):1772–1779PubMedCrossRefGoogle Scholar
  97. Sirota A, Csicsvari J et al (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci 100(4):2065–2069PubMedPubMedCentralCrossRefGoogle Scholar
  98. Sirota A, Montgomery S et al (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60(4):683–697PubMedPubMedCentralCrossRefGoogle Scholar
  99. Skaggs WE, McNaughton BL et al (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6(2):149–172PubMedCrossRefGoogle Scholar
  100. Squire LR, Genzel L et al (2015) Memory consolidation. Cold Spring Harb Perspect Biol 7(8):a021766PubMedCrossRefGoogle Scholar
  101. Staresina B, Bergmann TO et al (2015) “Hierachical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep.” Nat NeurosciGoogle Scholar
  102. Taxidis J, Anastassiou CA et al (2015) Local field potentials encode place cell ensemble activation during hippocampal sharp wave ripples. Neuron 87(3):590–604PubMedCrossRefGoogle Scholar
  103. Thierry AM, Gioanni Y et al (2000) Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 10(4):411–419PubMedCrossRefGoogle Scholar
  104. Tierney PL, Dégenètais E et al (2004) Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20(2):514–524PubMedCrossRefGoogle Scholar
  105. Tse D, Langston RF et al (2007) Schemas and memory consolidation. Science 316(5821):76–82PubMedCrossRefGoogle Scholar
  106. Tse D, Takeuchi T et al (2011) Schema-dependent gene activation and memory encoding in neocortex. Science 333(6044):891–895PubMedCrossRefGoogle Scholar
  107. van Buuren M, Kroes MC et al (2014) Initial investigation of the effects of an experimentally learned schema on spatial associative memory in humans. J Neurosci 34(50):16662–16670PubMedCrossRefGoogle Scholar
  108. van Kesteren MT, Fernandez G et al (2010a) Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci U S A 107(16):7550–7555PubMedPubMedCentralCrossRefGoogle Scholar
  109. van Kesteren MT, Rijpkema M et al (2010b) Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity. J Neurosci 30(47):15888–15894PubMedCrossRefGoogle Scholar
  110. van Kesteren MTR, Ruiter DJ et al (2012) How schema and novelty augment memory formation. Trends Neurosci 35(4):211–219PubMedCrossRefGoogle Scholar
  111. Varela C, Kumar S et al (2013) “Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens.” Brain Struct Funct 1–19Google Scholar
  112. Vertes RP (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142(1):1–20PubMedCrossRefGoogle Scholar
  113. Villette V, Malvache A et al (2015) Internally recurring hippocampal sequences as a population template of spatiotemporal information. Neuron 88(2):357–366PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wagner IC, van Buuren M et al (2015) “Schematic memory components converge within angular gyrus during retrieval.” Elife 4:e09668Google Scholar
  115. Wamsley EJ, Tucker MA et al (2012) Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry 71(2):154–161PubMedCrossRefGoogle Scholar
  116. Wang SH, Tse D et al (2012) Anterior cingulate cortex in schema assimilation and expression. Learn Mem 19(8):315–318PubMedPubMedCentralCrossRefGoogle Scholar
  117. Wang DV, Yau HJ et al (2015) Mesopontine median raphe regulates hippocampal ripple oscillation and memory consolidation. Nat Neurosci 18(5):728–735PubMedPubMedCentralCrossRefGoogle Scholar
  118. Wiltgen BJ, Zhou M et al (2010) The hippocampus plays a selective role in the retrieval of detailed contextual memories. Curr Biol 20(15):1336–1344PubMedPubMedCentralCrossRefGoogle Scholar
  119. Winocur G, Moscovitch M et al (2013) Factors affecting graded and ungraded memory loss following hippocampal lesions. Neurobiol Learn Mem 106:351–364PubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Centre for Cognitive and Neural SystemsUniversity of EdinburghEdinburghUK
  2. 2.Donders Institute for Brain Cognition and Behavior Radboud UniversiteitNijmegenThe Netherlands

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