In sync: Gamma oscillations and emotional memory

Frontiers in Behavioral Neuroscience

Volumn , Issue NOV, 2013, Pages

  Headley, Drew B ^a   Paré, Denis ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Amygdala; Arousal; Associative memory; Emotional memory; Gamma oscillations

Indexed keywords

ARTICLE; ASSOCIATIVE MEMORY; AVERSIVE BEHAVIOR; BASOLATERAL AMYGDALA; BRAIN REGION; ELECTROENCEPHALOGRAM; EMOTIONALITY; GAMMA RHYTHM; HUMAN; INTRACELLULAR SIGNALING; LATENT PERIOD; LEARNING; MEMORY; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OSCILLATION; PREDICTION; REWARD; STIMULUS RESPONSE;

EID: 84888324546     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00170     Document Type: Article

References (126)

1. Abeles, M. (1982). Role of the cortical neuron: integrator or coincidence detector?Isr. J. Med. Sci. 18, 83-92.
2. Albrecht, A., Çalişkan, G., Oitzl, M. S., Heinemann, U., and Stork, O. (2013). Long-lasting increase of corticosterone after fear memory reactivation: anxiolytic effects and network activity modulation in the ventral hippocampus. Neuropsychopharmacology 38, 386-394. doi: 10.1038/npp.2012.192.
3. Balconi, M., and Pozzoli, U. (2007). Event-related oscillations (EROs) and event-related potentials (ERPs) comparison in facial expression recognition. J. Neuropsychol. 1, 283-294. doi: 10.1348/174866407X184789.
4. Basar, E., Schmiedt-Fehr, C., Oniz, A., and Basar-Eroglu, C. (2008). Brain oscillations evoked by the face of a loved person. Brain Res. 1214, 105-115. doi: 10.1016/j.brainres.2008.03.042.
5. Bauer, E. P., Paz, R., and Pare, D. (2007). Gamma oscillations coordinate amygdalo-rhinal interactions during learning. J. Neurosci. 27, 9369-9379. doi: 10.1523/JNEUROSCI.2153-07.2007.
6. Bi, G. Q., and Poo, M. M. (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464-10472.
7. Boatman, J. A., and Kim, J. J. (2006). A thalamo-cortico-amygdala pathway mediates auditory fear conditioning in the intact brain. Eur. J. Neurosci. 24, 894-900. doi: 10.1111/j.1460-9568.2006.04965.x.
8. Borgers, C., Epstein, S., and Kopell, N. J. (2005). Background gamma rhythmicity and attention in cortical local circuits: a computational study. Proc. Natl. Acad. Sci. U.S.A. 102, 7002-7007. doi: 10.1073/pnas.0502366102.
9. Boring, E. G. (1936). Psychophysiological systems and isomorphic relations. Psychol. Rev. 43, 565-587. doi: 10.1037/h0059300.
10. Bradley, M. M., Greenwald, M. K., Petry, M. C., and Lang, P. J. (1992). Remembering pictures: pleasure and arousal in memory. J. Exp. Psychol. Learn. Mem. Cogn. 18, 379-390. doi: 10.1037/0278-7393.18.2.379.
11. Brown, S. P., and Hestrin, S. (2009). Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133-1136. doi: 10.1038/nature07658.
12. Buehlmann, A., and Deco, G. (2010). Optimal information transfer in the cortex through synchronization. PLoS Comput. Biol. 6:e1000934. doi: 10.1371/journal.pcbi.1000934.
13. Burt, D. B., Zembar, M. J., and Niederehe, G. (1995). Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity. Psychol. Bull. 117, 285-305. doi: 10.1037/0033-2909.117.2.285.
14. Buzsaki, G., and Wang, X. J. (2012). Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203-225. doi: 10.1146/annurev-neuro-062111-150444.
15. Cahill, L., and McGaugh, J. L. (1995). A novel demonstration of enhanced memory associated with emotional arousal. Conscious. Cogn. 4, 410-421. doi: 10.1006/ccog.1995.1048.
16. Christianson, S.-A., and Loftus, E. F. (1987). Memory for traumatic events. Oct-Dec 1987. Appl. Cogn. Psychol. 1, 225-239.
17. Colgin, L. L., and Moser, E. I. (2010). Gamma oscillations in the hippocampus. Physiology 25, 319-329. doi: 10.1152/physiol.00021.2010.
18. Collins, D. R., Pelletier, J. G., and Pare, D. (2001). Slow and fast (gamma) neuronal oscillations in the perirhinal cortex and lateral amygdala. J. Neurophysiol. 85, 1661-1672.
19. Csicsvari, J., Jamieson, B., Wise, K. D., and Buzsaki, G. (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311-322. doi: 10.1016/S0896-6273(02)01169-8.
20. Dringenberg, H. C., and Vanderwolf, C. H. (1996). Cholinergic activation of the electrocorticogram: an amygdaloid activating system. Exp. Brain. Res. 108, 285-296. doi: 10.1007/BF00228101.
21. Dumenko, V. N. (1995). Dynamic shifts in the parameters of the traditional frequency range of the EEG during learning in dogs. Neurosci. Behav. Physiol. 25, 403-412. doi: 10.1007/BF02359597.
22. Dzirasa, K., McGarity, D. L., Bhattacharya, A., Kumar, S., Takahashi, J. S., Dunson, D., et al. (2011). Impaired limbic gamma oscillatory synchrony during anxiety-related behavior in a genetic mouse model of bipolar mania. J. Neurosci. 31, 6449-6456. doi: 10.1523/JNEUROSCI.6144-10.2011.
23. Engel, A. K., Konig, P., Kreiter, A. K., and Singer, W. (1991a). Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252, 1177-1179. doi: 10.1126/science.252.5009.1177.
24. Engel, A. K., Kreiter, A. K., Konig, P., and Singer, W. (1991b). Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proc. Natl. Acad. Sci. U.S.A. 88, 6048-6052. doi: 10.1073/pnas.88.14.6048.
25. Fanselow, M. S., and Dong, H. W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19. doi: 10.1016/j.neuron.2009.11.031.
26. Fell, J., Klaver, P., Lehnertz, K., Grunwald, T., Schaller, C., Elger, C. E., et al. (2001). Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci. 4, 1259-1264. doi: 10.1038/nn759.
27. Fino, E., and Yuste, R. (2011). Dense inhibitory connectivity in neocortex. Neuron 69, 1188-1203. doi: 10.1016/j.neuron.2011.02.025.
28. Freeman, W. J. (1960). Correlation of elctrical activity of prepyriform cortex and behavior in cat. J Neurophysiol 23, 111-131.
29. Freiwald, W. A., Kreiter, A. K., and Singer, W. (1995). Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. Neuroreport 6, 2348-2352. doi: 10.1097/00001756-199511270-00018.
30. Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474-480. doi: 10.1016/j.tics.2005.08.011.
31. Fries, P., Reynolds, J. H., Rorie, A. E., and Desimone, R. (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560-1563. doi: 10.1126/science.1055465.
32. Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., et al. (2007). Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53, 591-604. doi: 10.1016/j.neuron.2007.01.031.
33. Galambos, R. (1992). "A comparison of certain gamma band (40-Hz) brain rhythms in cat and man, " in Induced Rhythms in the Brain, eds E. Basar and T. H. Bullock (Boston, MA: Springer Science).
34. Gibson, J. R., Beierlein, M., and Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79. doi: 10.1038/47035.
35. Glauser, E. S. D., and Scherer, K. R. (2008). Neuronal processes involved in subjective feeling emergence: oscillatory activity during an emotional monitoring task. Brain Topogr. 20, 224-231. doi: 10.1007/s10548-008-0048-3.
36. Gluck, H., and Rowland, V. (1959). Defensive conditioning of electrographic arousal with delayed and differentiated auditory stimuli. Electroencephalogr. Clin. Neurophysiol. 11, 485-496. doi: 10.1016/0013-4694(59)90047-1.
37. Gregoriou, G. G., Gotts, S. J., Zhou, H., and Desimone, R. (2009). High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science324, 1207-1210. doi: 10.1126/science.1171402.
38. Hasenstaub, A., Shu, Y., Haider, B., Kraushaar, U., Duque, A., and McCormick, D. A. (2005). Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47, 423-435. doi: 10.1016/j.neuron.2005.06.016.
39. Headley, D. B., and Weinberger, N. M. (2011). Gamma-band activation predicts both associative memory and cortical plasticity. J. Neurosci. 31, 12748-12758. doi: 10.1523/JNEUROSCI.2528-11.2011.
40. Headley, D. B., and Weinberger, N. M. (2013). Fear conditioning enhances gamma oscillations and their entrainment of neurons representing the conditioned stimulus.J. Neurosci. 33, 5705-5717. doi: 10.1523/JNEUROSCI.4915-12.2013.
41. Huff, M. L., Miller, R. L., Deisseroth, K., Moorman, D. E., and Lalumiere, R. T. (2013). Posttraining optogenetic manipulations of basolateral amygdala activity modulate consolidation of inhibitory avoidance memory in rats. Proc. Natl. Acad. Sci. U.S.A. 110, 3597-3602. doi: 10.1073/pnas.1219593110.
42. Izquierdo, I., Bevilaqua, L. R., Rossato, J. I., Bonini, J. S., Medina, J. H., and Cammarota, M. (2006). Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 29, 496-505. doi: 10.1016/j.tins.2006.07.005.
43. Jasper, H. H., and Andrews, H. L. (1938). Electroencephalography. III. Normal differentiation of occipital and precentral regions in man. Arch. Neurol. Psychiatry39, 96-115. doi: 10.1001/archneurpsyc.1938.02270010106010.
44. Jeschke, M., Lenz, D., Budinger, E., Herrmann, C. S., and Ohl, F. W. (2008). Gamma oscillations in gerbil auditory cortex during a target-discrimination task reflect matches with short-term memory. Brain Res. 1220, 70-80. doi: 10.1016/j.brainres.2007.10.047.
45. Jung, J., Bayle, D., Jerbi, K., Vidal, J. R., Henaff, M. A., Ossandon, T., et al. (2011). Intracerebral gamma modulations reveal interaction between emotional processing and action outcome evaluation in the human orbitofrontal cortex. Int. J. Psychophysiol. 79, 64-72. doi: 10.1016/j.ijpsycho.2010.09.014.
46. Jutras, M. J., Fries, P., and Buffalo, E. A. (2009). Gamma-band synchronization in the macaque hippocampus and memory formation. J. Neurosci. 29, 12521-12531. doi: 10.1523/JNEUROSCI.0640-09.2009.
47. Kanai, T., and Szerb, J. C. (1965). Mesencephalic reticular activating system and cortical acetylcholine output. Nature 205, 80-82. doi: 10.1038/205080b0.
48. Keil, A., Müller, M. M., Gruber, T., Wienbruch, C., Stolarova, M., and Elbert, T. (2001). Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials. Clin. Neurophysiol. 112, 2057-2068. doi: 10.1016/S1388-2457(01)00654-X.
49. Keil, A., Stolarova, M., Moratti, S., and Ray, W. J. (2007). Adaptation in human visual cortex as a mechanism for rapid discrimination of aversive stimuli. Neuroimage 36, 472-479. doi: 10.1016/j.neuroimage.2007.02.048.
50. Kensinger, E. A., and Schacter, D. L. (2008). "Memory and Emotion, " in Handbook of Emotions, eds M. Lewis, J. M. Haviland-Jones, and L. F. Barrett (New York, NY: The Guilford Press), 601-617.
51. Kimura, D. (1958). Effects of selective hippocampal damage on avoidance behaviour in the rat. Can. J. Psychol. 12, 213-218. doi: 10.1037/h0083740.
52. Kluver, H., and Bucy, P. C. (1939). Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiatry 42, 979-1000. doi: 10.1001/archneurpsyc.1939.02270240017001.
53. Konig, P., Engel, A. K., and Singer, W. (1996). Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130-137. doi: 10.1016/S0166-2236(96)80019-1.
54. Kuhn, A., Rotter, S., and Aertsen, A. (2002). Correlated input spike trains and their effects on the response of the leaky integrate-and-fire neuron. Neurocomputing 44, 121-126. doi: 10.1016/S0925-2312(02)00372-7.
55. Laitman, B. M., Dasilva, J. K., Ross, R. J., Tejani-Butt, S., and Morrison, A. R. (2011). Reduced gamma range activity at REM sleep onset and termination in fear-conditioned Wistar-Kyoto rats. Neurosci. Lett. 493, 14-17. doi: 10.1016/j.neulet.2011.02.003.
56. Lang, P. J., Bradley, M. M., and Cuthbert, B. N. (1999). International Affective Pictures System (IAPS): Instruction Manual and Affective Ratings. Technical Report A-8. Gainesville, FL: University of Florida.
57. Letzkus, J. J., Wolff, S. B., Meyer, E. M., Tovote, P., Courtin, J., Herry, C., et al. (2011). A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335. doi: 10.1038/nature10674.
58. Levy, R. B., and Reyes, A. D. (2012). Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex. J. Neurosci. 32, 5609-5619. doi: 10.1523/JNEUROSCI.5158-11.2012.
59. Levy, W. B., and Steward, O. (1983). Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8, 791-797. doi: 10.1016/0306-4522(83)90010-6.
60. Lu, C. B., Jefferys, G. R., Toescu, E. C., and Vreugdenhil, M. (2011). In vitrohippocampal gamma oscillation power as an index of in vivo CA3 gamma oscillation strength and spatial reference memory. Neurobiol. Learn. Mem. 95, 221-230. doi: 10.1016/j.nlm.2010.11.008.
61. Luo, Q., Holroyd, T., Jones, M., Hendler, T., and Blair, J. (2007). Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. Neuroimage 34, 839-847. doi: 10.1016/j.neuroimage.2006.09.023.
62. Luo, Q., Mitchell, D., Cheng, X., Mondillo, K., McCaffrey, D., Holroyd, T., et al. (2009). Visual awareness, emotion, and gamma band synchronization. Cereb. Cortex 19, 1896-1904. doi: 10.1093/cercor/bhn216.
63. Magoun, H. W. (1958). The Waking Brain. Springfield, IL: Charles C. Thomas. doi: 10.1037/11149-000.
64. Markram, H., Lubke, J., Frotscher, M., and Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215. doi: 10.1126/science.275.5297.213.
65. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807. doi: 10.1038/nrn1519.
66. Martin, S. J., Grimwood, P. D., and Morris, R. G. M. (2000). Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 659-711. doi: 10.1146/annurev.neuro.23.1.649.
67. Martinez, J. L. Jr., and Derrick, B. E. (1996). Long-term potentiation and learning. Annu. Rev. Psychol. 47, 173-203. doi: 10.1146/annurev.psych.47.1.173.
68. Martini, N., Menicucci, D., Sebastiani, L., Bedini, R., Pingitore, A., Vanello, N., et al. (2012). The dynamics of EEG gamma responses to unpleasant visual stimuli: from local activity to functional connectivity. Neuroimage 60, 922-932. doi: 10.1016/j.neuroimage.2012.01.060.
69. Mather, M., and Sutherland, M. R. (2011). Arousal-biased competition in perception and memory. Perspect. Psychol. Sci. 6, 114-133. doi: 10.1177/1745691611400234.
70. Matsumoto, A., Ichikawa, Y., Kanayama, N., Ohira, H., and Iidaka, T. (2006). Gamma band activity and its synchronization reflect the dysfunctional emotional processing in alexithymic persons. Psychophysiology 43, 533-540. doi: 10.1111/j.1469-8986.2006.00461.x.
71. McCormick, D. A., Connors, B. W., Lighthall, J. W., and Prince, D. A. (1985). Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54, 782-806.
72. McGaugh, J. L. (2000). Memory-a century of consolidation. Science 287, 248-251. doi: 10.1126/science.287.5451.248.
73. McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1-28. doi: 10.1146/annurev.neuro.27.070203.144157.
74. McLin, D. E. 3rd. Miasnikov, A. A., and Weinberger, N. M. (2002). Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. U.S.A. 99, 4002-4007. doi: 10.1073/pnas.062057099.
75. McLin, D. E. 3rd. Miasnikov, A. A., and Weinberger, N. M. (2003). CS-specific gamma, theta, and alpha EEG activity detected in stimulus generalization following induction of behavioral memory by stimulation of the nucleus basalis. Neurobiol. Learn. Mem. 79, 152-176. doi: 10.1016/S1074-7427(02)00009-6.
76. Mesulam, M. M., Mufson, E. J., Wainer, B. H., and Levey, A. I. (1983). Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10, 1185-1201. doi: 10.1016/0306-4522(83)90108-2.
77. Metherate, R., Cox, C. L., and Ashe, J. H. (1992). Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701-4711.
78. Miasnikov, A. A., Chen, J. C., Gross, N., Poytress, B. S., and Weinberger, N. M. (2008). Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory. Neurobiol. Learn. Mem. 90, 125-137. doi: 10.1016/j.nlm.2008.02.001.
79. Miltner, W. H., Braun, C., Arnold, M., Witte, H., and Taub, E. (1999). Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397, 434-436. doi: 10.1038/17126.
80. Molle, M., Marshall, L., Gais, S., and Born, J. (2004). Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc. Natl. Acad. Sci. U.S.A. 101, 13963-13968. doi: 10.1073/pnas.0402820101.
81. Morrell, F. (1961). Electrophysiological contributions to the neural basis of learning. Physiol. Rev. 41, 443-494.
82. Moruzzi, G., and Magoun, H. W. (1949). Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455-473.
83. Müller, G. E., and Pilzecker, A. (1900). Experimentelle Beitrage zur Lehre vom Gedachtnis. Z. Psychol. Erganzungsband 1, 1-300.
84. Müller, M. M., Keil, A., Gruber, T., and Elbert, T. (1999). Processing of affective pictures modulates right-hemispheric gamma band EEG activity. Clin. Neurophysiol. 110, 1913-1920. doi: 10.1016/S1388-2457(99)00151-0.
85. Oathes, D. J., Ray, W. J., Yamasaki, A. S., Borkovec, T. D., Castonguay, L. G., Newman, M. G., et al. (2008). Worry, generalized anxiety disorder, and emotion: evidence from the EEG gamma band. Biol. Psychol. 79, 165-170. doi: 10.1016/j.biopsycho.2008.04.005.
86. Osipova, D., Takashima, A., Oostenveld, R., Fernandez, G., Maris, E., and Jensen, O. (2006). Theta and gamma oscillations predict encoding and retrieval of declarative memory. J. Neurosci. 26, 7523-7531. doi: 10.1523/JNEUROSCI.1948-06.2006.
87. Oswald, A. M., Doiron, B., Rinzel, J., and Reyes, A. D. (2009). Spatial profile and differential recruitment of GABAB modulate oscillatory activity in auditory cortex. J. Neurosci. 29, 10321-10334. doi: 10.1523/JNEUROSCI.1703-09.2009.
88. Oya, H., Kawasaki, H., Howard, M. A. 3rd., and Adolphs, R. (2002). Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J. Neurosci. 22, 9502-9512.
89. Packer, A. M., and Yuste, R. (2011). Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J. Neurosci. 31, 13260-13271. doi: 10.1523/JNEUROSCI.3131-11.2011.
90. Pagano, R. R., and Gault, F. P. (1964). Amygdala activity: a central measure of arousal. Electroencephalogr. Clin. Neurophysiol. 17, 255-260. doi: 10.1016/0013-4694(64)90126-9.
91. Paller, K. A., and Wagner, A. D. (2002). Observing the transformation of experience into memory. Trends Cogn. Sci. 6, 93-102. doi: 10.1016/S1364-6613(00)01845-3.
92. Parikh, V., Kozak, R., Martinez, V., and Sarter, M. (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56, 141-154. doi: 10.1016/j.neuron.2007.08.025.
93. Pavlov, I. P. (1927). Conditioned Reflexes. New York, NY: Dover.
94. Perin, R., Berger, T. K., and Markram, H. (2011). A synaptic organizing principle for cortical neuronal groups. Proc. Natl. Acad. Sci. U.S.A. 108, 5419-5424. doi: 10.1073/pnas.1016051108.
95. Pfaus, J. G., Kippin, T. E., and Centeno, S. (2001). Conditioning and sexual behavior: a review. Horm. Behav. 40, 291-321. doi: 10.1006/hbeh.2001.1686.
96. Popa, D., Duvarci, S., Popescu, A. T., Lena, C., and Pare, D. (2010). Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl. Acad. Sci. U.S.A. 107, 6516-6519. doi: 10.1073/pnas.0913016107.
97. Popescu, A. T., Popa, D., and Pare, D. (2009). Coherent gamma oscillations couple the amygdala and striatum during learning. Nat. Neurosci. 12, 801-807. doi: 10.1038/nn.2305.
98. Power, A. E., Roozendaal, B., and McGaugh, J. L. (2000). Glucocorticoid enhancement of memory consolidation in the rat is blocked by muscarinic receptor antagonism in the basolateral amygdala. Eur. J. Neurosci. 12, 3481-3487. doi: 10.1046/j.1460-9568.2000.00224.x.
99. Randall, F. E., Whittington, M. A., and Cunningham, M. O. (2011). Fast oscillatory activity induced by kainate receptor activation in the rat basolateral amygdala in vitro. Eur. J. Neurosci. 33, 914-922. doi: 10.1111/j.1460-9568.2010.07582.x.
100. Rapaport, D. (1971). Emotions and Memory. New York, NY: International University Press, Inc.
101. Rheinberger, M. B., and Jasper, H. H. (1937). Electrical activity of the cerebral cortex in the unanesthetized cat. Am. J. Physiol. 119, 186-196.
102. Romanski, L. M., and Ledoux, J. E. (1992). Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J. Neurosci. 12, 4501-4509.
103. Salinas, E., and Sejnowski, T. J. (2000). Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20, 6193-6209.
104. Sato, W., Kochiyama, T., Uono, S., Matsuda, K., Usui, K., Inoue, Y., et al. (2011). Rapid amygdala gamma oscillations in response to fearful facial expressions. Neuropsychologia 49, 612-617. doi: 10.1016/j.neuropsychologia.2010.12.025.
105. Sederberg, P. B., Kahana, M. J., Howard, M. W., Donner, E. J., and Madsen, J. R. (2003). Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 23, 10809-10814.
106. Sederberg, P. B., Schulze-Bonhage, A., Madsen, J. R., Bromfield, E. B., McCarthy, D. C., Brandt, A., et al. (2007). Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex 17, 1190-1196. doi: 10.1093/cercor/bhl030.
107. Senkowski, D., Kautz, J., Hauck, M., Zimmermann, R., and Engel, A. K. (2011). Emotional facial expressions modulate pain-induced beta and gamma oscillations in sensorimotor cortex. J. Neurosci. 31, 14542-14550. doi: 10.1523/JNEUROSCI.6002-10.2011.
108. Siegle, G. J., Condray, R., Thase, M. E., Keshavan, M., and Steinhauer, S. R. (2010). Sustained gamma-band EEG following negative words in depression and schizophrenia. Int. J. Psychophysiol. 75, 107-118. doi: 10.1016/j.ijpsycho.2008.04.008.
109. Sinfield, J. L., and Collins, D. R. (2006). Induction of synchronous oscillatory activity in the rat lateral amygdala in vitro is dependent on gap junction activity. Eur. J. Neurosci. 24, 3091-3095. doi: 10.1111/j.1460-9568.2006.05202.x.
110. Sohal, V. S., Zhang, F., Yizhar, O., and Deisseroth, K. (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702. doi: 10.1038/nature07991.
111. Sokolov, E. N., and Vinogradova, O. S. (1975). Neuronal Mechanisms of the Orienting Reflex. New York, NY: L. Erlbaum Associates.
112. Squire, L. R., and Cohen, N. (1979). Memory and amnesia: resistance to disruption develops for years after learning. Behav. Neural Biol. 25, 115-125. doi: 10.1016/S0163-1047(79)90841-0.
113. Steriade, M., and Amzica, F. (1996). Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc. Natl. Acad. Sci. U.S.A. 93, 2533-2538. doi: 10.1073/pnas.93.6.2533.
114. Steriade, M., Amzica, F., and Contreras, D. (1996). Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J. Neurosci. 16, 392-417.
115. Sukov, W., and Barth, D. S. (1998). Three-dimensional analysis of spontaneous and thalamically evoked gamma oscillations in auditory cortex. J. Neurophysiol. 79, 2875-2884.
116. Tallon-Baudry, C., and Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3, 151-162. doi: 10.1016/S1364-6613(99)01299-1.
117. Teyler, T. J. (1971). Effects of restraint on heart-rate conditioning in rats as a function of US location. J. Comp. Physiol. Psychol. 77, 31-37. doi: 10.1037/h0031579.
118. Volgushev, M., Chistiakova, M., and Singer, W. (1998). Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83, 15-25. doi: 10.1016/S0306-4522(97)00380-1.
119. Wang, X. J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90, 1195-1268. doi: 10.1152/physrev.00035.2008.
120. Weinberger, N. M. (2004). Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5, 279-290. doi: 10.1038/nrn1366.
121. Weinberger, N. M., Javid, R., and Lepan, B. (1993). Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 90, 2394-2398. doi: 10.1073/pnas.90.6.2394.
122. Wespatat, V., Tennigkeit, F., and Singer, W. (2004). Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex. J. Neurosci. 24, 9067-9075. doi: 10.1523/JNEUROSCI.2221-04.2004.
123. Whittington, M. A., Cunningham, M. O., Lebeau, F. E., Racca, C., and Traub, R. D. (2011). Multiple origins of the cortical gamma rhythm. Dev. Neurobiol. 71, 92-106. doi: 10.1002/dneu.20814.
124. Womelsdorf, T., Schoffelen, J. M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., et al. (2007). Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609-1612. doi: 10.1126/science.1139597.
125. Yerkes, R. M., and Dodson, J. D. (1908). The relation of strength of stimulus to rapidity of habit formation. J. Comp. Neurol. 18, 459-482. doi: 10.1002/cne.920180503.
126. Yuval-Greenberg, S., Tomer, O., Keren, A. S., Nelken, I., and Deouell, L. Y. (2008). Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron 58, 429-441. doi: 10.1016/j.neuron.2008.03.027.