New technologies for examining the role of neuronal ensembles in drug addiction and fear

Nature Reviews Neuroscience

Volumn 14, Issue 11, 2013, Pages 743-754

  Cruz, Fabio C ^a   Koya, Eisuke ^a,b   Guez Barber, Danielle H ^a,c   Bossert, Jennifer M ^a   Lupica, Carl R ^a   Shaham, Yavin ^a   Hope, Bruce T ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLATOSTATIN; BACLOFEN; BETA GALACTOSIDASE; COCAINE; DAUNORUBICIN; DIAMORPHINE; DIPHTHERIA TOXIN; MUSCIMOL; PROTEIN FOS; TRANSCRIPTION FACTOR FOSB; YOHIMBINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASSOCIATION; BASOLATERAL AMYGDALA; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CELL DEATH; COMPARATIVE STUDY; CONDITIONED REFLEX; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; DRUG DEPENDENCE; DRUG EFFECT; DRUG EXPOSURE; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; DRUG USE; EPIFLUORESCENCE MICROSCOPY; FEAR; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; INSTRUMENTAL CONDITIONING; LATERAL AMYGDALA; LEARNING; LOCOMOTION; MEMORY; MOUSE; NERVE CELL; NERVE CELL CHARACTERISTICS AND FUNCTIONS; NERVE CELL PLASTICITY; NEURONAL ENSEMBLE; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; ORBITAL CORTEX; PHENOTYPE; PLACE PREFERENCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROMOTER REGION; RELAPSE; REWARD; SENSITIZATION; SYNAPTIC EFFICACY; WITHDRAWAL SYNDROME;

ANIMALS; BRAIN; CONDITIONING (PSYCHOLOGY); DOPAMINE; FEAR; GENES, IMMEDIATE-EARLY; HUMANS; LIMBIC SYSTEM; MICE; NEURONS; RATS; REWARD; SUBSTANCE-RELATED DISORDERS;

MUS MUSCULUS; RATTUS;

EID: 84886085321     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3597     Document Type: Article

References (144)

1. Hebb, D. O. The Organization of Behavior: a Neuropsychological Theory (Wiley, 1949).
2. Schwindel, C. D. & McNaughton, B. L. Hippocampal-cortical interactions and the dynamics of memory trace reactivation. Prog. Brain Res. 193, 163-177 (2011).
3. Nicolelis, M. A., Fanselow, E. E. & Ghazanfar, A. A. Hebb's dream: the resurgence of cell assemblies. Neuron 19, 219-221 (1997). (Pubitemid 27374221)
4. Guzowski, J. F., Knierim, J. J. & Moser, E. I. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 44, 581-584 (2004). (Pubitemid 39531222)
5. Pennartz, C. M., Groenewegen, H. J. & Lopes da Silva, F. H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol. 42, 719-761 (1994). (Pubitemid 24199524)
6. Knierim, J. J. & Zhang, K. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35, 267-285 (2012).
7. Buzsaki, G. & Moser, E. I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neurosci. 16, 130-138 (2013).
8. Penner, M. R. & Mizumori, S. J. Neural systems analysis of decision making during goal-directed navigation. Prog. Neurobiol. 96, 96-135 (2012).
9. Mountcastle, V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20, 408-434 (1957).
10. John, E. R. & Schwartz, E. L. The neurophysiology of information processing and cognition. Annu. Rev. Psychol. 29, 1-29 (1978).
11. O'Keefe, J. A review of the hippocampal place cells. Prog. Neurobiol. 13, 419-439 (1979). (Pubitemid 10140563)
12. Carelli, R. M. & Deadwyler, S. A. Cellular mechanisms underlying reinforcement-related processing in the nucleus accumbens: electrophysiological studies in behaving animals. Pharmacol. Biochem. Behav. 57, 495-504 (1997). (Pubitemid 27296761)
13. Maren, S. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24, 897-931 (2001).
14. Guzowski, J. F., McNaughton, B. L., Barnes, C. A. & Worley, P. F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nature Neurosci. 2, 1120-1124 (1999). (Pubitemid 30126371)
15. Mattson, B. J. et al. Context-specific sensitization of cocaine-induced locomotor activity and associated neuronal ensembles in rat nucleus accumbens. Eur. J. Neurosci. 27, 202-212 (2008).
16. Reijmers, L. G., Perkins, B. L., Matsuo, N. & Mayford, M. Localization of a stable neural correlate of associative memory. Science 317, 1230-1233 (2007).
17. Guzowski, J. F. et al. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 15, 599-606 (2005). (Pubitemid 41394406)
18. Garner, A. & Mayford, M. New approaches to neural circuits in behavior. Learn. Mem. 19, 385-390 (2012).
19. Liu, X. et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484, 381-385 (2012).
20. Grienberger, C. & Konnerth, A. Imaging calcium in neurons. Neuron 73, 862-885 (2012).
21. Harvey, C. D., Collman, F., Dombeck, D. A. & Tank, D. W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946 (2009).
22. Ziv, Y. et al. Long-term dynamics of CA1 hippocampal place codes. Nature Neurosci. 16, 264-266 (2013).
23. Rogan, S. C. & Roth, B. L. Remote control of neuronal signaling. Pharmacol. Rev. 63, 291-315 (2011).
24. Sweatt, J. D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76, 1-10 (2001).
25. Alberini, C. M. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci. 28, 51-56 (2005). (Pubitemid 40038802)
26. Tronson, N. C. & Taylor, J. R. Molecular mechanisms of memory reconsolidation. Nature Rev. Neurosci. 8, 262-275 (2007). (Pubitemid 46452320)
27. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M. & Deisseroth, K. Optogenetics in neural systems. Neuron 71, 9-34 (2011).
28. Koya, E. et al. Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nature Neurosci. 12, 1069-1073 (2009).
29. Guez-Barber, D. et al. FACS identifies unique cocaine-induced gene regulation in selectively activated adult striatal neurons. J. Neurosci. 31, 4251-4259 (2011).
30. Cifani, C. et al. Medial prefrontal cortex neuronal activation and synaptic alterations after stress-induced reinstatement of palatable food seeking: a study using c-fos-GFP transgenic female rats. J. Neurosci. 32, 8480-8490 (2012).
31. Han, J. H. et al. Selective erasure of a fear memory. Science 323, 1492-1496 (2009).
32. Zhou, Y. et al. CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nature Neurosci. 12, 1438-1443 (2009).
33. Garner, A. R. et al. Generation of a synthetic memory trace. Science 335, 1513-1516 (2012).
34. Morgan, J. I. & Curran, T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14, 421-451 (1991).
35. Cohen, S. & Greenberg, M. E. Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol. 24, 183-209 (2008).
36. Herdegen, T. & Leah, J. D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 28, 370-490 (1998). (Pubitemid 29012678)
37. Goldberg, S. R. Stimuli associated with drug injections as events that control behavior. Pharmacol. Rev. 27, 325-340 (1976).
38. Stewart, J., de Wit, H. & Eikelboom, R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol. Rev. 91, 251-268 (1984).
39. O'Brien, C. P., Ehrman, R. N. & Ternes, J. W. in Behavioral Analysis of Drug Dependence (eds Goldberg, S. & Stolerman, I.) 329-356 (Academic Press, 1986).
40. Wikler, A. Dynamics of drug dependence. Implications of a conditioning theory for research and treatment. Arch. Gen. Psychiatry 28, 611-616 (1973).
41. Siegel, S. Drug anticipation and drug addiction. The 1998 H. David Archibald Lecture. Addiction 94, 1113-1124 (1999). (Pubitemid 29385140)
42. Carelli, R. M. The nucleus accumbens and reward: neurophysiological investigations in behaving animals. Behav. Cogn. Neurosci. Rev. 1, 281-296 (2002).
43. Rebec, G. V. & Sun, W. Neuronal substrates of relapse to cocaine-seeking behavior: role of prefrontal cortex. J. Exp. Anal. Behav. 84, 653-666 (2005). (Pubitemid 43339129)
44. Schuster, C. R. & Thompson, T. Self administration of and behavioral dependence on drugs. Annu. Rev. Pharmacol. 9, 483-502 (1969).
45. Chang, J. Y., Zhang, L., Janak, P. H. & Woodward, D. J. Neuronal responses in prefrontal cortex and nucleus accumbens during heroin self-administration in freely moving rats. Brain Res. 754, 12-20 (1997). (Pubitemid 27170246)
46. Kiyatkin, E. A. & Rebec, G. V. Activity of presumed dopamine neurons in the ventral tegmental area during heroin self-administration. Neuroreport 8, 2581-2585 (1997). (Pubitemid 27308465)
47. Carelli, R. M., King, V. C., Hampson, R. E. & Deadwyler, S. A. Firing patterns of nucleus accumbens neurons during cocaine self-administration in rats. Brain Res. 626, 14-22 (1993). (Pubitemid 23306806)
48. Peoples, L. L. & West, M. O. Phasic firing of single neurons in the rat nucleus accumbens correlated with the timing of intravenous cocaine self-administration. J. Neurosci. 16, 3459-3473 (1996). (Pubitemid 26142375)
49. Carelli, R. M., Williams, J. G. & Hollander, J. A. Basolateral amygdala neurons encode cocaine self-administration and cocaine-associated cues. J. Neurosci. 23, 8204-8211 (2003). (Pubitemid 37129636)
50. Root, D. H., Fabbricatore, A. T., Ma, S., Barker, D. J. & West, M. O. Rapid phasic activity of ventral pallidal neurons during cocaine self-administration. Synapse 64, 704-713 (2010).
51. Bowers, M. S., Chen, B. T. & Bonci, A. AMPA receptor synaptic plasticity induced by psychostimulants: the past, present, and therapeutic future. Neuron 67, 11-24 (2010).
52. Russo, S. J. et al. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267-276 (2010).
53. Wolf, M. E. & Ferrario, C. R. AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci. Biobehav. Rev. 35, 185-211 (2010).
54. Thomas, M. J., Kalivas, P. W. & Shaham, Y. Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br. J. Pharmacol. 154, 327-342 (2008). (Pubitemid 351670603)
55. Kalivas, P. W. & Volkow, N. D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 162, 1403-1413 (2005). (Pubitemid 41105554)
56. Shaham, Y. & Hope, B. T. The role of neuroadaptations in relapse to drug seeking. Nature Neurosci. 8, 1437-1439 (2005). (Pubitemid 41573651)
57. Mameli, M. & Luscher, C. Synaptic plasticity and addiction: learning mechanisms gone awry. Neuropharmacology 61, 1052-1059 (2011).
58. Shaham, Y., Shalev, U., Lu, L., De Wit, H. & Stewart, J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168, 3-20 (2003). (Pubitemid 36851158)
59. Marchant, N. J., Li, X. & Shaham, Y. Recent developments in animal models of drug relapse. Curr. Opin. Neurobiol. 23, 675-683 (2013).
60. Pickens, C. L. et al. Neurobiology of incubation of drug craving. Trends Neurosci. 34, 411-420 (2011).
61. Kasof, G. M. et al. Spontaneous and evoked glutamate signalling influences Fos-lacZ expression and pyramidal cell death in hippocampal slice cultures from transgenic rats. Brain Res. Mol. Brain Res. 34, 197-208 (1995). (Pubitemid 26007076)
62. Kasof, G. M. et al. Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats. J. Neurosci. 15, 4238-4249 (1995).
63. Kasof, G. M., Smeyne, R. J., Curran, T. & Morgan, J. I. Developmental expression of Fos-lacZ in the brains of postnatal transgenic rats. Brain Res. Dev. Brain Res. 93, 191-197 (1996). (Pubitemid 26188998)
64. Bakina, E. & Farquhar, D. Intensely cytotoxic anthracycline prodrugs: galactosides. Anticancer Drug Des. 14, 507-515 (1999). (Pubitemid 30258970)
65. Farquhar, D. et al. Suicide gene therapy using E. coli β-galactosidase. Cancer Chemother. Pharmacol. 50, 65-70 (2002). (Pubitemid 34743998)
66. Ghosh, A. K., Khan, S., Marini, J., Nelson, J. C. & Farquhar, D. A daunorubicin β-galactoside prodrug for use in conjunction with gene-directed enzyme prodrug therapy. Tetrahedron Lett. 41, 4871-4874 (2000). (Pubitemid 30431119)
67. Bossert, J. M. et al. Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nature Neurosci. 14, 420-422 (2011).
68. Fanous, S. et al. Role of orbitofrontal cortex neuronal ensembles in the expression of incubation of heroin craving. J. Neurosci. 32, 11600-11609 (2012).
69. Santone, K. S., Oakes, S. G., Taylor, S. R. & Powis, G. Anthracycline-induced inhibition of a calcium action potential in differentiated murine neuroblastoma cells. Cancer Res. 46, 2659-2664 (1986). (Pubitemid 16074258)
70. Badiani, A. & Robinson, T. E. Drug-induced neurobehavioral plasticity: the role of environmental context. Behav. Pharmacol. 15, 327-339 (2004). (Pubitemid 39238343)
71. Stewart, J. & Badiani, A. Tolerance and sensitization to the behavioral effects of drugs. Behav. Pharmacol. 4, 289-312 (1993). (Pubitemid 23258353)
72. Mullen, R. J., Buck, C. R. & Smith, A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211 (1992).
73. Crombag, H., Bossert, J. M., Koya, E. & Shaham, Y. Context-induced relapse to drug seeking: a review. Trans. R. Soc. B 363, 3233-3243 (2008).
74. Grimm, J. W., Hope, B. T., Wise, R. A. & Shaham, Y. Incubation of cocaine craving after withdrawal. Nature 412, 141-142 (2001). (Pubitemid 32674700)
75. Shalev, U., Morales, M., Hope, B., Yap, J. & Shaham, Y. Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology 156, 98-107 (2001). (Pubitemid 32646331)
76. Neisewander, J. L. et al. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J. Neurosci. 20, 798-805 (2000). (Pubitemid 30225582)
77. Lobo, M. K. Molecular profiling of striatonigral and striatopallidal medium spiny neurons past, present, and future. Int. Rev. Neurobiol. 89, 1-35 (2009).
78. Lobo, M. K., Karsten, S. L., Gray, M., Geschwind, D. H. & Yang, X. W. FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nature Neurosci. 9, 443-452 (2006). (Pubitemid 43290975)
79. Dougherty, J. D. & Geschwind, D. H. Progress in realizing the promise of microarrays in systems neurobiology. Neuron 45, 183-185 (2005). (Pubitemid 40128111)
80. Karsten, S. L., Kudo, L. C. & Geschwind, D. H. Gene expression analysis of neural cells and tissues using DNA microarrays. Curr. Protoc. Neurosci. 45, 4.28.1-4.28.38 (2008).
81. Guez-Barber, D. et al. FACS purification of immunolabeled cell types from adult rat brain. J. Neurosci. Methods 203, 10-18 (2012).
82. Fanous, S. et al. Unique gene alterations are induced in FACS-purified Fos-positive neurons activated during cue-induced relapse to heroin seeking. J. Neurochem. 124, 100-108 (2013).
83. Everitt, B. J. & Robbins, T. W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nature Neurosci. 8, 1481-1489 (2005). (Pubitemid 41573659)
84. Kelley, A. E. & Berridge, K. C. The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci. 22, 3306-3311 (2002). (Pubitemid 37465733)
85. Ikemoto, S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78 (2007). (Pubitemid 350110353)
86. Liu, Q. R. et al. Detection of molecular alterations in methamphetamine-activated Fos-expressing neurons from a single rat dorsal striatum using fluorescence-activated cell sorting (FACS). J. Neurochem. http://dx.doi.org/10.1111/jnc.12381 (2013).
87. Bredt, D. S. & Nicoll, R. A. AMPA receptor trafficking at excitatory synapses. Neuron 40, 361-379 (2003). (Pubitemid 37244101)
88. Martin, S. J., Grimwood, P. D. & Morris, R. G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711 (2000). (Pubitemid 30350057)
89. Luscher, C. & Malenka, R. C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650-663 (2011).
90. Benedetti, B. L., Takashima, Y., Wen, J. A., Urban-Ciecko, J. & Barth, A. L. Differential wiring of layer 2/3 neurons drives sparse and reliable firing during neocortical development. Cereb. Cortex http://dx.doi.org/10.1093/ cercor/bhs257 (2012).
91. Clem, R. L. & Barth, A. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663-670 (2006). (Pubitemid 43290126)
92. Barth, A. L. Visualizing circuits and systems using transgenic reporters of neural activity. Curr. Opin. Neurobiol. 17, 567-571 (2007).
93. Barth, A. L., Gerkin, R. C. & Dean, K. L. Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J. Neurosci. 24, 6466-6475 (2004). (Pubitemid 38971693)
94. Yassin, L. et al. An embedded subnetwork of highly active neurons in the neocortex. Neuron 68, 1043-1050 (2010).
95. Koya, E. et al. Silent synapses in selectively activated nucleus accumbens neurons following cocaine sensitization. Nature Neurosci. 15, 1556-1562 (2012).
96. Isaac, J. T., Crair, M. C., Nicoll, R. A. & Malenka, R. C. Silent synapses during development of thalamocortical inputs. Neuron 18, 269-280 (1997). (Pubitemid 27111109)
97. Brown, T. E. et al. A silent synapse-based mechanism for cocaine-induced locomotor sensitization. J. Neurosci. 31, 8163-8174 (2011).
98. Huang, Y. H. et al. In vivo cocaine experience generates silent synapses. Neuron 63, 40-47 (2009).
99. Nair, S. G., Adams-Deutsch, T., Epstein, D. H. & Shaham, Y. The neuropharmacology of relapse to food seeking: methodology, main findings, and comparison with relapse to drug seeking. Prog. Neurobiol. 89, 18-45 (2009).
100. Ghitza, U. E., Gray, S. M., Epstein, D. H., Rice, K. C. & Shaham, Y. The anxiogenic drug yohimbine reinstates palatable food seeking in a rat relapse model: a role of CRF1 receptors. Neuropsychopharmacology 31, 2188-2196 (2006). (Pubitemid 44413196)
101. Nair, S. G. et al. Role of dorsal medial prefrontal cortex dopamine D1-family receptors in relapse to high-fat food seeking induced by the anxiogenic drug yohimbine. Neuropsychopharmacology 36, 497-510 (2011).
102. Calu, D. J. et al. Optogenetic inhibition of dorsal medial prefrontal cortex attenuates stress-induced reinstatement of palatable food seeking in female rats. J. Neurosci. 33, 214-226 (2013).
103. Bremner, J. D., Krystal, J. H., Southwick, S. M. & Charney, D. S. Noradrenergic mechanisms in stress and anxiety: II. clinical studies. Synapse 23, 39-51 (1996). (Pubitemid 26138646)
104. Ungless, M. A., Whistler, J. L., Malenka, R. C. & Bonci, A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583-587 (2001). (Pubitemid 32531404)
105. Mennerick, S. & Zorumski, C. F. Paired-pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons. J. Physiol. 488, 85-101 (1995).
106. Quirk, G. J. & Mueller, D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33, 56-72 (2008). (Pubitemid 350191313)
107. Pape, H. C. & Pare, D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 90, 419-463 (2010).
108. Paz, R. & Pare, D. Physiological basis for emotional modulation of memory circuits by the amygdala. Curr. Opin. Neurobiol. 23, 381-386 (2013).
109. Barot, S. K., Chung, A., Kim, J. J. & Bernstein, I. L. Functional imaging of stimulus convergence in amygdalar neurons during Pavlovian fear conditioning. PLoS ONE 4, e6156 (2009).
110. Chung, A., Barot, S. K., Kim, J. J. & Bernstein, I. L. Biologically predisposed learning and selective associations in amygdalar neurons. Learn. Mem. 18, 371-374 (2011).
111. Hashikawa, K., Matsuki, N. & Nomura, H. Preferential Arc transcription at rest in the active ensemble during associative learning. Neurobiol. Learn. Mem. 95, 498-504 (2011).
112. Purgert, R. J., Wheeler, D. S., McDannald, M. A. & Holland, P. C. Role of amygdala central nucleus in aversive learning produced by shock or by unexpected omission of food. J. Neurosci. 32, 2461-2472 (2012).
113. Josselyn, S. A. Continuing the search for the engram: examining the mechanism of fear memories. J. Psychiatry Neurosci. 35, 221-228 (2010).
114. Reijmers, L. & Mayford, M. Genetic control of active neural circuits. Front. Mol. Neurosci. 2, 27 (2009).
115. Alexander, G. M. et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63, 27-39 (2009).
116. Tayler, K. K., Tanaka, K. Z., Reijmers, L. G. & Wiltgen, B. J. Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr. Biol. 23, 99-106 (2013).
117. Han, J. H. et al. Neuronal competition and selection during memory formation. Science 316, 457-460 (2007).
118. Dong, Y. et al. CREB modulates excitability of nucleus accumbens neurons. Nature Neurosci. 9, 475-477 (2006).
119. Marie, H., Morishita, W., Yu, X., Calakos, N. & Malenka, R. C. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 741-752 (2005). (Pubitemid 40320708)
120. Guenthner, C. J., Miyamichi, K., Yang, H. H., Heller, H. C. & Luo, L. Permanent genetic access to transiently active neurons via TRAP: targeted recombination in active populations. Neuron 78, 773-784 (2013).
121. Peter, M. et al. Transgenic mouse models enabling photolabeling of individual neurons in vivo. PLoS ONE 8, e62132 (2013).
122. Sanders, J., Cowansage, K., Baumgartel, K. & Mayford, M. Elimination of dendritic spines with long-term memory is specific to active circuits. J. Neurosci. 32, 12570-12578 (2012).
123. Matsuo, N., Reijmers, L. & Mayford, M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319, 1104-1107 (2008). (Pubitemid 351300794)
124. Cao, V. Y. et al. In vivo two-photon imaging of experience-dependent molecular changes in cortical neurons. J. Vis. Exp. 71, e50148 (2013).
125. Kawashima, T. et al. Synaptic activity-responsive element in the Arc/Arg-3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl Acad. Sci. USA 106, 316-321 (2009).
126. Johnson, J. W. & Kotermanski, S. E. Mechanism of action of memantine. Curr. Opin. Pharmacol. 6, 61-67 (2006). (Pubitemid 43103820)
127. Sinner, B. & Graf, B. M. Ketamine. Handb. Exp. Pharmacol. 182, 313-333 (2008).
128. Wood, P. L. The NMDA receptor complex: a long and winding road to therapeutics. IDrugs 8, 229-235 (2005).
129. Nader, K., Schafe, G. E. & LeDoux, J. E. The labile nature of consolidation theory. Nature Rev. Neurosci. 1, 216-219 (2000).
130. Lerea, L. S., Butler, L. S. & McNamara, J. O. NMDA and non-NMDA receptor-mediated increase of c-fos mRNA in dentate gyrus neurons involves calcium influx via different routes. J. Neurosci. 12, 2973-2981 (1992).
131. Sgambato, V., Abo, V., Rogard, M., Besson, M. J. & Deniau, J. M. Effect of electrical stimulation of the cerebral cortex on the expression of the Fos protein in the basal ganglia. Neuroscience 81, 93-112 (1997). (Pubitemid 27373631)
132. Vazdarjanova, A. & Guzowski, J. F. Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J. Neurosci. 24, 6489-6496 (2004). (Pubitemid 38971696)
133. Hope, B. T. et al. Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron 13, 1235-1244 (1994). (Pubitemid 24372141)
134. Sheng, M. & Greenberg, M. E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4, 477-485 (1990). (Pubitemid 20160837)
135. Hardingham, G. E., Chawla, S., Johnson, C. M. & Bading, H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260-265 (1997). (Pubitemid 27043726)
136. Valjent, E., Caboche, J. & Vanhoutte, P. Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain: a molecular substrate for learning and memory? Mol. Neurobiol. 23, 83-99 (2001). (Pubitemid 33030093)
137. Thomas, G. M. & Huganir, R. L. MAPK cascade signalling and synaptic plasticity. Nature Rev. Neurosci. 5, 173-183 (2004). (Pubitemid 38252474)
138. Mattson, B. J. et al. Cocaine-induced CREB phosphorylation in nucleus accumbens of cocaine-sensitized rats is enabled by enhanced activation of extracellular signal-related kinase, but not protein kinase A. J. Neurochem. 95, 1481-1494 (2005). (Pubitemid 41779271)
139. LaHoste, G. J., Yu, J. & Marshall, J. F. Striatal Fos expression is indicative of dopamine D1/D2 synergism and receptor supersensitivity. Proc. Natl Acad. Sci. USA 90, 7451-7455 (1993). (Pubitemid 23249967)
140. Hardingham, G. E., Arnold, F. J. & Bading, H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nature Neurosci. 4, 261-267 (2001). (Pubitemid 32194873)
141. Deisseroth, K., Mermelstein, P. G., Xia, H. & Tsien, R. W. Signaling from synapse to nucleus: the logic behind the mechanisms. Curr. Opin. Neurobiol. 13, 354-365 (2003). (Pubitemid 36805579)
142. O'Donnell, P. Dopamine gating of forebrain neural ensembles. Eur. J. Neurosci. 17, 429-435 (2003). (Pubitemid 36255880)
143. Labiner, D. M. et al. Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J. Neurosci. 13, 744-751 (1993). (Pubitemid 23045155)
144. Kreuter, J. D., Mattson, B. J., Wang, B., You, Z. B. & Hope, B. T. Cocaine-induced Fos expression in rat striatum is blocked by chloral hydrate or urethane. Neuroscience 127, 233-242 (2004). (Pubitemid 38829168)