Part 2:What Is Neural Codes Of Memory During Sleep?
Mar 10, 2022
For more information:ali.ma@wecistganche.com
Contextual memory
All memories are context-specific, whether being spatial, temporal or emotional, leading to the concept of sequence coding or trajectory coding. As the hippocampal network is connected with the amygdala— a specific brain area responsible for emotions and memory modulation, episodic memories are often associated with emotions, such as happiness, fear, and anxiety. This may occur in memory recall and dream experiences. Notably, sleep consolidates or reshapes emotional memories [97]. One hypothesis is that emotional or contextual memory can be strengthened or weakened in the hippocampus during REM sleep theta activity [98,99]. Recent causal evidence showed that temporally precise attenuation of the theta rhythm impaired fear-conditioned contextual memory [99]. However, how to read out contextual episodic memories embedded with distinct emotions is still a big puzzle. The development of new computational approaches for deciphering hippocampal-amygdala population codes will be an extended research direction.
Click to cistanche tubulosa dosage and Cistanche for improving memory
Creativity and insight
Creativity involves the forming of associative elements into novel associations that are useful for future task behaviors (e.g., planning, problem solving). Such new association patterns might not occur frequently, and shall not be confused with the “preplay” events [100]. Insight is defined as a neural restructuring process that leads to a sudden gain of explicit knowledge leading to qualitatively changed behavior [101]. Human sleep studies suggested that REM sleep promotes creativity and insight because ofthe changes in cholinergic and noradrenergic neuromodulation [102], which allow neocortical structures to reorganize associative hierarchies and reinterpret the hippocampal information. Computationally, how to detect such new associations of spatiotemporal patterns across a large hippocampal-neocortical network remains unknown. Future simultaneous recordings from multiple targeted brain areas would enable us to examine high-dimensional spatiotemporal spike patterns and evaluate their probabilities of coincident reactivations at different brain states.
Manipulation of memory
To date, neuroscientists have relied on many powerful engineering or genetic tools, such as the virtual environment [103, 104] and optogenetics [53, 105– 108], to manipulate hippocampal memory during wakeful experiences. In virtual environments, rodent hippocampal neurons exhibited different spike firing patterns from real environments. However, it remains unclear how such firing patterns would be affected in sleep. False memories play a significant role in human mental health and legal practice [109]. In a series of groundbreaking experiments [105, 106], researchers stimulated or suppressed memories with optogenetics to manipulate engram-bearing neurons in the mouse hippocampus. Their findings suggested that optogenetic reactivation of memory engram-bearing cells was not only sufficient for the behavioral recall ofthat memory, but also served as a conditioned stimulus for the formation of an associative memory. Techniques of selective enhancement of desired memories and indirect suppression of unwanted memories might find potential translational applications in treating traumatic memories in post-traumatic stress disorder (PTSD) patients. Similarly, it remains unknown how these manipulations affect memory during sleep. Among all experimental manipulations, one key research goal is to study their sleep-associated memory contents and use them to further predict future behavior.
Closed-loop neural interface
Brain-machine interfaces provide not only potential therapies for animals and humans, but also new tools for studying memory processing during sleep [44,53, 110, 111]. Combining various invasive (e.g., electrical) or non-invasive (e.g., optical, acoustic) closed-loop stimulation techniques [39, 112– 115], we can test the causal functions of neural circuits or sleep for memory processing in a real-time manner. For instance, coupling spontaneous reactivation of a place cell during sleep to a reinforcing stimulation ofthe medial forebrain bundle (MFB) induced a place preference during subsequent wake, providing another evidence that place cells encode the same spatial information during sleep and wakefulness [116].
Concluding Remarks
In summary, accumulative experimental evidence has pinpointed the critical role of sleep in consolidating hippocampal-neocortical memories. With advances in large-scale neural population recordings and imaging techniques, it is imperative to develop computationally relevant methods to provide unbiased assessment of memory-related SANC. Despite rapid progress in the last two decades, many outstanding questions still remain. Furthermore, contributions of many other subcortical circuits to various sleep-associated memories remain to be investigated, such as the ventral striatum [117, 118] and the anterior thalamus [119, 120]. Combinations of experimental and computational investigations will be a crucial step forward for improving our understanding ofthis exciting and important research field. Future dissection of memory during sleep will shed light on neural mechanisms of dreaming, creativity, contextual or emotional memories, and will provide further insights into memory-related neurological and psychiatric disorders.
Acknowledgments
We thank B. Bagnasacco, F. Kloosterman and B. Pesaran for valuable comments. This work is supported by an NSF/NIH CRCNS award IIS-1307645 (to Z.C. and M.A.W.) from the US National Science Foundation, an NSF/NIH CRCNS award R01-NS100065 (to Z.C.) from the NINDS, the Office ofNaval Research MURI grant N00014-10-1-0936 and an NIH grant TR01-GM104948 (to M.A.W.). This material is also based upon work supported by the Center for Brains, Minds and Machines (CBMM), funded by NSF STC award CCF-1231216.
Glossary
Episodic Memory
is made of associations of several elements, such as objects, space and times. The associations are encoded by chemical and physical changes in neurons, as well as by modifications to synapses between neurons
Hippocampus
a brain structure within the medial temporal lobe (MTL) that is important for episodic memory, spatial learning and associative recollection. It consists of CA1, CA2, CA3 and dental gyrus, and is connected to various brain structures, including the prefrontal cortex (PFC), entorhinal cortex and amygdala
Memory Consolidation
a process that converts and stabilizes information from short-term memory into long-term storage. The hippocampal-neocortical memory consolidation involves transferring hippocampal episodic memory into the neocortex during the off-line (such as sleep) process after waking experiences in memory acquisition
Population Codes
are referred to neuronal ensemble spike activity that represents and transmits information. Spikes are the basic neuronal language for information and communication. Depending on specific neural circuits, different statistical assumptions are made about the computational principle or information carrier, such as spike count, spike timing, independent or correlation codes
UP and DOWN States
are defined as periods (~a few hundred milliseconds) of synchronized population firing and widespread depolarization, and periods of relative silence and hyperpolarization, respectively. The DOWN states alternate between the UP states during slow wave sleep
Local Field Potential (LFP)
is considered to represent the aggregate subthreshold activity of a local population of neurons in a spatially localized area near the recording electrode and can be viewed as the input information in that area. Spectral analysis ofthe broadband LFP signal can reveal significant oscillatory activity at specific frequency bands
Rapid Eye Movement (REM) Sleep
a sleep stage characterized by quick, random movements ofthe eyes and low muscle tone. REM sleep occurs in cycles of about 90–120 minutes in night and accounts for 20–30% sleep time in adult humans. Most human dream activity occurs in REM sleep. In rodents, REM sleep is accompanied by theta oscillations
Slow Wave Sleep (SWS)
a sleep stage also known as non-REM (NREM) sleep or deep sleep, accounting for ~75% of total sleep time, is characterized by synchronized EEG activity of slow waves with frequency below 1 Hz and relatively high amplitude. Sleep spindles (9–15 Hz) occur during
Place Receptive Field (RF)
a property of localized spatial tuning exhibited prominently in hippocampal pyramidal neurons of rodents and bats. The RF defines the firing property of hippocampal place cells with respect to specific spatial location. On a linear track, the rodent hippocampal place RF is often directionally dependent
False Memory
refers to recall of an event or observation that did not actually occur. Internally generated stimuli can get associated with concurrent external stimuli, which can lead to the formation of false memories
References
1. Andersen, P., et al. The Hippocampus Book. Oxford University Press; 2006.
2. Stickgold R. Sleep-dependent memory consolidation. Nature. 2005; 437:1272–1278. [PubMed: 16251952]
3. Marshall L, Born J. Contribution of sleep to hippocampus-dependent memory consolidation. Trends Cog Sci. 2007; 11:442–450.
4. Buzsaki G. Memory consolidation during sleep: a neurophysiology perspective. J Sleep Res. 1998; 7:17–23. [PubMed: 9682189]
5. Breton J, Robertson EM. Memory processing: The critical role of neuronal replay during sleep. Curr Biol. 2013; 23:R836–R838. [PubMed: 24070442]
6. Rasch B, Born J. About sleep’s role in memory. Physiol Rev. 2013; 93:681–766. [PubMed: 23589831]
7. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010; 11:114–126. [PubMed: 20046194]
8. Pavlides C, Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989; 9:2907–2918. [PubMed: 2769370]
9. Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994; 265:676–679. [PubMed: 8036517]
10. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996; 271:1870–1873. [PubMed: 8596957]
11. Kudrimoti HS, et al. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999; 19:4090–4101. [PubMed: 10234037]
12. Nadasdy Z, et al. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999; 19:9497–9507. [PubMed: 10531452]
13. Dang-Vu TT, et al. Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci USA. 2008; 105:15160–15165. [PubMed: 18815373]
14. Rudoy JD, et al. Strengthening individual memories by reactivating them during sleep. Science. 2009; 1079
15. Fuentemilla L, et al. Hippocampal-dependent strengthening of targeted memories via reactivation during sleep in humans. Curr Biol. 2013; 23:1769–1775. [PubMed: 24012316]
16. Staresina BP, et al. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci. 2015; 18:1679–1686. [PubMed: 26389842]
17. Buzsaki G, Mizuseki K. The log-dynamic brain: how skewed distributions affect network operations. Nat Rev Neurosci. 2014; 26:88–95.
18. Colgin LL. Rhythms ofthe hippocampal network. Nat Rev Neurosci. 2016; 17:239–249. [PubMed: 26961163]
19. Steriade M, et al. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol. 2001; 85:1969–1985. [PubMed: 11353014]
20. Battaglia FP, et al. Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem. 2004; 22:697–704.
21. Haggerty DC, Ji D. Initiation of sleep-dependent cortical-hippocampal correlations at wakefulness- sleep transition. J Neurophysiol. 2014; 112:1763–1774. [PubMed: 25008411]
22. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971; 34:171–175. [PubMed: 5124915]
23. Eichenbaum H, et al. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron. 1999; 23:209–226. [PubMed: 10399928]
24. Allen TA, et al. Nonspatial sequence coding in CA1 neuron. J Neurosci. 2016; 36:1547–1563. [PubMed: 26843637]
25. Shan KQ, et al. Spatial tuning and brain state account for dorsal hippocampal CA1 activity in a non-spatial learning task. eLife. 2016; 5:e14321. [PubMed: 27487561]
26. Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002; 36:1183–1194. [PubMed: 12495631]
27. Roumis DK, Frank LM. Hippocampal sharp-wave ripples in waking and sleep states. Curr Opin Neurobiol. 2015; 35:6–12. [PubMed: 26011627]
28. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in place cells during the awake state. Nature. 2006; 440:680–683. [PubMed: 16474382]
29. Diba K, Buzsaki G. Forward and reverse hippocampal place-cell sequence during ripples. Nat Neurosci. 2007; 10:1241–1242. [PubMed: 17828259]
30. Vyazovskiy VV, et al. Local sleep in awake rats. Nature. 2011; 472:443–447. [PubMed: 21525926]
31. Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001; 29:145–156. [PubMed: 11182087]
32. Lee AK, Wilson MA. A combinatorial method for analyzing sequential firing patterns involving an arbitrary number ofneurons based on relative time order. J Neurophysiol. 2004; 92:2555–2573. [PubMed: 15212425]
33. Siapas AG, Wilson MA. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron. 1998; 21:1123–1128. [PubMed: 9856467]
34. Sirota A, et al. Commmunication between neocortex and hippocampus during sleep in rodents. Proc Nat Acad Sci USA. 2003; 100:2065–2069. [PubMed: 12576550]
35. Wang SH, Morris RG. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Ann Rev Psychol. 2010; 61:49–79. [PubMed: 19575620]
36. Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007; 10:100–107. [PubMed: 17173043]
37. Bendor D, Wilson MA. Biasing the content of hippocampal replay during sleep. Nat Neurosci. 2012; 15:1439–1444. [PubMed: 22941111]
38. Rothschild G, et al. A cortical-hippocampal-cortical loop of information processing during memory consolidation. Nat Neurosci. 2017; 20:251–259. [PubMed: 27941790]
39. Maingret N, et al. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat Neurosci. 2016; 19:959–964. [PubMed: 27182818]
40. Ribeiro S, et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2004; 2:126–137.
41. Qin YL, et al. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Phil Trans R Sco Lond Ser B. 1997; 352:1525–1533.
42. Euston DR, et al. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science. 2007; 318:1147–1150. [PubMed: 18006749]
43. Peyrache A, et al. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci. 2009; 12:919–926. [PubMed: 19483687]
44. Gulati T, et al. Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning. Nat Neurosci. 2014; 17:1107–1113. [PubMed: 24997761]
45. Ramanthan DS, et al. Sleep-dependent reactivation of ensembles in motor cortex promotes skill consolidation. PLoS Biol. 2015; 13:e1002263. [PubMed: 26382320]
46. O’Neill J, et al. Superficial layers of the medial entorhinal cortex replay independently ofthe hippocampus. Science. 2017; 355:184–188. [PubMed: 28082591]
47. Dave AS, Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science. 2000; 290:812–816. [PubMed: 11052946]
48. Hoffman KL, McNaughton BL. Coordinated reactivation of distributed memory traces in primate neocortex. Science. 2002; 297:2070–2073. [PubMed: 12242447]
49. Olafsdottir HF, et al. Coordinated grid and place cell replay during rest. Nat Neursci. 2016; 19:792–794.
50. Davidson TJ, et al. Hippocampal replay of extended experience. Neuron. 2009; 63:497–507. [PubMed: 19709631]
51. Giradeau G, et al. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 2009; 12:1222–1223. [PubMed: 19749750]
52. Ego-Stengel V, Wilson MA. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus. 2010; 20:1–10. [PubMed: 19816984]
53. va den Ven GM, et al. Hippocampal offline reactivation consolidates recently formed cell assembly patterns during sharp wave-ripples. Neuron. 2016; 92:968–974. [PubMed: 27840002]
54. Corkin S. What’s new with the amnesic patient H.M.? Nat Rev Neurosci. 2002; 3:153–160. [PubMed: 11836523]
55. Nir Y, et al. Regional slow waves and spindles in human sleep. Neuron. 2011; 70:153–169. [PubMed: 21482364]
56. Horikawa T, et al. Neural decoding of visual imagery during sleep. Science. 2013; 340:639–642. [PubMed: 23558170]
57. Andrillon T, et al. Single-neuron activity and eye movements during human REM sleep and wake vision. Nat Commu. 2015; 6:7884.
58. Peyrache A, et al. Principal component analysis of ensemble recordings reveal cell assemblies at high temporal resolution. J Comput Neurosci. 2010; 29:309–325. [PubMed: 19529888]
59. Lopes-dos-Santos V, et al. Detecting cell assemblies in large neuronal populations. J Neurosci Meth. 2013; 220:149–166.
60. Dabaghian Y, et al. Reconceiving the hippocampal map as a topological template. eLife. 2014; 3:e03476. [PubMed: 25141375]
61. Giusti C, et al. Clique topology reveals intrinsic geometric structure in neural correlations. Proc Nat Acad Sci USA. 2015; 112:13455–13460. [PubMed: 26487684]
62. Curto C. What can topology tell us about the neural code? Bull Amer Math Soc. 2017; 54:63–78.
63. Quiroga RQ, Panzeri S. Extracting information from neuronal populations: information theory and decoding approaches. Nat Rev Neurosci. 2009; 10:173–185. [PubMed: 19229240]
64. Brown EN, et al. A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci. 1998; 18:7411–7425. [PubMed: 9736661]
65. Zhang K, et al. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J Neurophysiol. 1998; 79:1017–1044. [PubMed: 9463459]
66. Chen Z, et al. Uncovering spatial topology represented by hippocampal population codes. J Comput Neurosci. 2012; 33:1–29. [PubMed: 22089473]
67. Chen Z, et al. Neural representation of spatial topology in the rodent hippocampus. Neural Comput. 2014; 26:1–39. [PubMed: 24102128]
68. Linderman SW, et al. A Bayesian nonparametric approach to uncovering rat hippocampal population codes during spatial navigation. J Neurosci Methods. 2016; 263:36–47. [PubMed: 26854398]
69. Chen Z, et al. Uncovering representations of sleep-associated hippocampal ensemble spike activity. Sci Rep. 2016; 6:32193. [PubMed: 27573200]
70. Velluti RA. Interactions between sleep and sensory physiology. J Sleep Res. 1997; 6:61–77. [PubMed: 9377536]
71. Wood ER, et al. The global record of memory in hippocampal neuronal activity. Nature. 1999; 397:613–616. [PubMed: 10050854]
72. Hampson RE, et al. Distribution of spatial and nonspatial information in dorsal hippocampus. Nature. 1999; 402:610–614. [PubMed: 10604466]
73. Cohen SJ, et al. The rodent hippocampus is essential for nonspatial object memory. Curr Biol. 2013; 23:1685–1690. [PubMed: 23954431]
74. Takahashi S. Hierarchical organization of context in the hippocampal episodic code. eLife. 2013; 2:e00321. [PubMed: 23390588]
75. Grosmark AD, Buzsáki G. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. Science. 2016; 351:1440–1443. [PubMed: 27013730]
76. Vyazovskiy VV, et al. Cortical firing and sleep homeostasis. Neuron. 2009; 63:865–878. [PubMed: 19778514]
77. Watson BO, et al. Network homeostasis and state dynamics of neocortical sleep. Neuron. 2016; 90:839–852. [PubMed: 27133462]
78. Stevenson IH, Kording KP. How advances in neural recording affect data analysis. Nat Neurosci. 2011; 14:139–142. [PubMed: 21270781]
79. Berenyi A, et al. Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. J Neurophysiol. 2014; 111:1132–1149. [PubMed: 24353300]
80. Micho F, et al. Integration of silicon-based neural probes and micro-drive arrays for the chronic recording of large populations of neurons in behaving animals. J Neural Eng. 2016; 13:046018. [PubMed: 27351591]
81. Rios G, et al. Nanofabricated neural probes for dense 3-D recordings of brain activity. NANO Lett. 2016; 16:6857–6862. [PubMed: 27766885]
82. Ziv Y, et al. Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci. 2013; 16:264–266. [PubMed: 23396101]
83. Rubin A, et al. Hippocampal ensemble dynamics timestamp events in long-term memory. eLife. 2015; 4:e12247. [PubMed: 26682652]
84. Villette V, et al. Internally recurring hippocampal sequences as a population template of spatiotemporal information. Neuron. 2015; 88:357–366. [PubMed: 26494280]
85. Malvache A, et al. Awake hippocampal reactivation project onto orthogonal neuronal assemblies. Science. 2016; 353:1280–1283. [PubMed: 27634534]
86. Niethard N, et al. Sleep-stage-specific regulation of cortical excitation and inhibition. Curr Biol. 2016; 26:2739–2749. [PubMed: 27693142]
87. Logothetis NK, et al. Hippocampal-cortical interaction during periods of subcortical silence. Nature. 2012; 491:547–553. [PubMed: 23172213]
88. Yin M, et al. Wireless neurosensory for full-spectrum electrophysiology recordings during free behavior. Neuron. 2014; 84:1170–1182. [PubMed: 25482026]
89. Siegel JM. The REM sleep-memory consolidation hypothesis. Science. 2001; 294:1058–1064. [PubMed: 11691984]
90. Vertes RP. Memory consolidation in sleep: dream or reality. Neuron. 2004; 44:135–148. [PubMed: 15450166]
91. Grosmark AD, et al. REM sleep reorganizes hippocampal excitability. Neuron. 2012; 75:1001–1007. [PubMed: 22998869]
92. Poe GR, et al. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Research. 2000; 855:176–180. [PubMed: 10650147]
93. Crick F, Mitchison G. The function of dream sleep. Nature. 1983; 304:111–114. [PubMed: 6866101]
94. Jego S, et al. Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat Neurosci. 2013; 16:1637–1643. [PubMed: 24056699]
95. Van Dort CJ, et al. Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep. Proc Natl Acad Sci USA. 2015; 112:584–589. [PubMed: 25548191]
96. Weber F, Dan Y. Circuit-based interrogation of sleep control. Nature. 2016; 538:51–59. [PubMed: 27708309]
97. Payne JD, Kensinger EA. Sleep’s role in the consolidation of emotional episodic memories. Curr Directions Psych Sci. 2010; 19:290–295.
98. Hutchison IC, Rathore S. The role ofREM sleep theta activity in emotional memory. Front Psychol. 2015; 6:1439. [PubMed: 26483709]
99. Boyce R, et al. Causal evidence for the role ofREM sleep theta rhythm in contextual memory consolidation. Science. 2016; 352:812–816. [PubMed: 27174984]
100. Dragoi G, Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature. 2011; 469:391–401.
101. Wagner U, et al. Sleep inspires insight. Nature. 2004; 427:352–355. [PubMed: 14737168]
102. Cai DJ, et al. REM, not incubation, improves creativity by priming associative network. Proc Nat Acad Sci USA. 2009; 106:10130–10134. [PubMed: 19506253]
103. Ravassar P, et al. Multisensory control of hippocampal spatiotemporal selectivity. Science. 2013; 340:1342–1346. [PubMed: 23641063]
104. Chen G, et al. How vision and movement combine in the hippocampal place code. Proc Natl Acad Sci USA. 2013; 110:378–383. [PubMed: 23256159]
105. Liu X, et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature. 2012; 484:381–385. [PubMed: 22441246]
106. Ramirez S, et al. Creating a false memory in the hippocampus. Science. 2013; 341:387–391. [PubMed: 23888038]
107. Redondo RL, et al. Bidirectional switch ofthe valence associated with a hippocampal contextual memory engram. Nature. 2014; 513:426–430. [PubMed: 25162525]
108. Tonegawa S, et al. Memory engram cells have come of age. Neuron. 2015; 87:918–931. [PubMed: 26335640]
109. Loftus E. Planting misinformation in the human mind: A 30-year investigation ofthe malleability of memory. Learning & Memory. 2005; 12:361–366. [PubMed: 16027179]
110. Marshall L, et al. Boosting slow oscillations during sleep potentiates memory. Nature. 2006; 444:610–613. [PubMed: 17086200]
111. Harris KD. Sleep replay meets brain-machine interface. Nat Neurosci. 2014; 17:1019–1021. [PubMed: 25065437]
112. Ngo HVV, et al. Auditory closed-loop stimulation ofthe sleep slow oscillation enhances memory. Neuron. 2013; 78:545–553. [PubMed: 23583623]
113. Jadhav SP, et al. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2013; 336:1454–1458.
114. Siegle JH, Wilson MA. Enhancement of encoding and retrieval functions through theta phase- specific manipulation of hippocampus. eLife. 2014; 3:e03061. [PubMed: 25073927]
115. Talakoub O, et al. Closed-loop interruption of hippocampal ripples through fornix stimulation in the non-human primate. Brain Stimulation. 2013; 9:911–918.
116. de Lvilleon G, et al. Explicit memory creation during sleep demonstrates a causal role of place cells in navigation. Nat Neurosci. 2015; 18:493–495. [PubMed: 25751533]
117. Pennartz CM, et al. The ventral striatum inn off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci. 2004; 24:6446–6456. [PubMed: 15269254]
118. Lansink CS, et al. Preferential reactivation of motivationally relevant information in the ventral striatum. J Neurosci. 2008; 28:6372–6382. [PubMed: 18562607]
119. Wolff M, et al. Beyond spatial memory: the anterior thalamus and memory for the temporal order of a sequence of odor cues. J Neurosci. 2006; 26:2907–2913. [PubMed: 16540567]
120. Magnin M, et al. Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc Nat Acad Sci USA. 2009; 107:3829–3833.
