Neural Representations of Unconditioned Stimuli in Basolateral Amygdala Mediate Innate and Learned Responses

Cell

Volumn 162, Issue 1, 2015, Pages 134-145

  Gore, Felicity ^a   Schwartz, Edmund C ^a   Brangers, Baylor C ^a   Aladi, Stanley ^a   Stujenske, Joseph M ^a   Likhtik, Ekaterina ^a   Russo, Marco J ^a   Gordon, Joshua A ^a,c   Salzman, C Daniel ^a,c   Axel, Richard ^a,b  

^a Howard Hughes Medical Institute   (United States)

^b Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE;

ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL AMYGDALA; CONDITIONED REFLEX; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; EMOTION; FOOTSHOCK; INSTRUMENTAL CONDITIONING; LEARNING; MALE; MOUSE; NONHUMAN; PHOTOACTIVATION; PLACE PREFERENCE; PRIORITY JOURNAL; STATE DEPENDENT LEARNING; UNCONDITIONED STIMULI; ANIMAL; ANIMAL BEHAVIOR; APPETITE; C57BL MOUSE; PHYSIOLOGY; REWARD;

ANIMALS; APPETITIVE BEHAVIOR; BASOLATERAL NUCLEAR COMPLEX; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; LEARNING; MALE; MICE; MICE, INBRED C57BL; REWARD;

EID: 84934267798     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.06.027     Document Type: Article

References (74)

1. T. Amano, S. Duvarci, D. Popa, and D. Paré The fear circuit revisited: contributions of the basal amygdala nuclei to conditioned fear J. Neurosci. 31 2011 15481 15489
2. D. Amaral, J. Price, A. Pitkanen, and S. Carmichael The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction J. Aggleton, 1992 Wiley-Liss New York 1 66
3. F. Ambroggi, A. Ishikawa, H.L. Fields, and S.M. Nicola Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons Neuron 59 2008 648 661
4. D. Anglada-Figueroa, and G.J. Quirk Lesions of the basal amygdala block expression of conditioned fear but not extinction J. Neurosci. 25 2005 9680 9685
5. B.W. Balleine, and S. Killcross Parallel incentive processing: an integrated view of amygdala function Trends Neurosci. 29 2006 272 279
6. S.K. Barot, Y. Kyono, E.W. Clark, and I.L. Bernstein Visualizing stimulus convergence in amygdala neurons during associative learning Proc. Natl. Acad. Sci. USA 105 2008 20959 20963
7. D.A. Belkin Bradycardia in response to threat Am. Zool. 8 1968 775
8. M.A. Belova, J.J. Paton, S.E. Morrison, and C.D. Salzman Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala Neuron 55 2007 970 984
9. M.A. Belova, J.J. Paton, and C.D. Salzman Moment-to-moment tracking of state value in the amygdala J. Neurosci. 28 2008 10023 10030
10. M.A. Bermudez, and W. Schultz Reward magnitude coding in primate amygdala neurons J. Neurophysiol. 104 2010 3424 3432
11. P. Blundell, G. Hall, and S. Killcross Lesions of the basolateral amygdala disrupt selective aspects of reinforcer representation in rats J. Neurosci. 21 2001 9018 9026
12. R.N. Cardinal, J.A. Parkinson, J. Hall, and B.J. Everitt Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex Neurosci. Biobehav. Rev. 26 2002 321 352
13. G.B. Choi, D.D. Stettler, B.R. Kallman, S.T. Bhaskar, A. Fleischmann, and R. Axel Driving opposing behaviors with ensembles of piriform neurons Cell 146 2011 1004 1015
14. L.H. Corbit, and B.W. Balleine Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer J. Neurosci. 25 2005 962 970
15. M. Davis Anatomic and physiologic substrates of emotion in an animal model J. Clin. Neurophysiol. 15 1998 378 387
16. B.J. Everitt, R.N. Cardinal, J.A. Parkinson, and T.W. Robbins Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning Ann. N Y Acad. Sci. 985 2003 233 250
17. M.S. Fanselow Conditioned and unconditional components of post-shock freezing Pavlov. J. Biol. Sci. 15 1980 177 182
18. A.C. Felix-Ortiz, A. Beyeler, C. Seo, C.A. Leppla, C.P. Wildes, and K.M. Tye BLA to vHPC inputs modulate anxiety-related behaviors Neuron 79 2013 658 664
19. M. Fendt, and M.S. Fanselow The neuroanatomical and neurochemical basis of conditioned fear Neurosci. Biobehav. Rev. 23 1999 743 760
20. M. Gallagher, and P.C. Holland The amygdala complex: multiple roles in associative learning and attention Proc. Natl. Acad. Sci. USA 91 1994 11771 11776
21. J.F. Guzowski, and P.F. Worley Cellular compartment analysis of temporal activity by fluorescence in situ hybridization (catFISH) Curr. Protoc. Neurosci. Chapter 1 2001 10.1002/0471142301.ns0108s15 Unit 1.8
22. T. Hatfield, J.S. Han, M. Conley, M. Gallagher, and P. Holland Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects J. Neurosci. 16 1996 5256 5265
23. C. Herry, S. Ciocchi, V. Senn, L. Demmou, C. Müller, and A. Lüthi Switching on and off fear by distinct neuronal circuits Nature 454 2008 600 606
24. P.C. Holland Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: implications for behavior theory Anim. Learn. Behav. 25 1997 373 399
25. P.C. Holland Event representation in Pavlovian conditioning: image and action Cognition 37 1990 105 131
26. K.R. Illig, and L.B. Haberly Odor-evoked activity is spatially distributed in piriform cortex J. Comp. Neurol. 457 2003 361 373
27. P.H. Janak, and K.M. Tye From circuits to behaviour in the amygdala Nature 517 2015 284 292
28. J.P. Johansen, H. Hamanaka, M.H. Monfils, R. Behnia, K. Deisseroth, H.T. Blair, and J.E. LeDoux Optical activation of lateral amygdala pyramidal cells instructs associative fear learning Proc. Natl. Acad. Sci. USA 107 2010 12692 12697
29. J.P. Johansen, C.K. Cain, L.E. Ostroff, and J.E. LeDoux Molecular mechanisms of fear learning and memory Cell 147 2011 509 524
30. S.Y. Kim, A. Adhikari, S.Y. Lee, J.H. Marshel, C.K. Kim, C.S. Mallory, M. Lo, S. Pak, J. Mattis, and B.K. Lim Diverging neural pathways assemble a behavioural state from separable features in anxiety Nature 496 2013 219 223
31. E. Knapska, K. Radwanska, T. Werka, and L. Kaczmarek Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse Physiol. Rev. 87 2007 1113 1173
32. P.J. Lang, and M. Davis Emotion, motivation, and the brain: reflex foundations in animal and human research Prog. Brain Res. 156 2006 3 29
33. J.E. LeDoux Emotion circuits in the brain Annu. Rev. Neurosci. 23 2000 155 184
34. U. Livneh, and R. Paz Aversive-bias and stage-selectivity in neurons of the primate amygdala during acquisition, extinction, and overnight retention J. Neurosci. 32 2012 8598 8610
35. M.B. Luskin, and J.L. Price The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb J. Comp. Neurol. 216 1983 264 291
36. S. Maren, and G.J. Quirk Neuronal signalling of fear memory Nat. Rev. Neurosci. 5 2004 844 852
37. S. Maren, S.A. Yap, and K.A. Goosens The amygdala is essential for the development of neuronal plasticity in the medial geniculate nucleus during auditory fear conditioning in rats J. Neurosci. 21 2001 RC135
38. A.J. McDonald Cortical pathways to the mammalian amygdala Prog. Neurobiol. 55 1998 257 332
39. L.L. Merritt, B.R. Martin, C. Walters, A.H. Lichtman, and M.I. Damaj The endogenous cannabinoid system modulates nicotine reward and dependence J. Pharmacol. Exp. Ther. 326 2008 483 492
40. S.E. Morrison, A. Saez, B. Lau, and C.D. Salzman Different time courses for learning-related changes in amygdala and orbitofrontal cortex Neuron 71 2011 1127 1140
41. K. Muramoto, T. Ono, H. Nishijo, and M. Fukuda Rat amygdaloid neuron responses during auditory discrimination Neuroscience 52 1993 621 636
42. P. Namburi, A. Beyeler, S. Yorozu, G.G. Calhoon, S.A. Halbert, R. Wichmann, S.S. Holden, K.L. Mertens, M. Anahtar, and A.C. Felix-Ortiz A circuit mechanism for differentiating positive and negative associations Nature 520 2015 675 678
43. H.C. Pape, and D. Paré Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear Physiol. Rev. 90 2010 419 463
44. J.J. Paton, M.A. Belova, S.E. Morrison, and C.D. Salzman The primate amygdala represents the positive and negative value of visual stimuli during learning Nature 439 2006 865 870
45. I.P. Pavlov Conditioned Reflexes 1927 Oxford University Press London
46. C.L. Pickens, and P.C. Holland Conditioning and cognition Neurosci. Biobehav. Rev. 28 2004 651 661
47. G.J. Quirk, C. Repa, and J.E. LeDoux Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat Neuron 15 1995 1029 1039
48. R.L. Redondo, J. Kim, A.L. Arons, S. Ramirez, X. Liu, and S. Tonegawa Bidirectional switch of the valence associated with a hippocampal contextual memory engram Nature 513 2014 426 430
49. R.L. Rennaker, C.F. Chen, A.M. Ruyle, A.M. Sloan, and D.A. Wilson Spatial and temporal distribution of odorant-evoked activity in the piriform cortex J. Neurosci. 27 2007 1534 1542
50. J.C. Repa, J. Muller, J. Apergis, T.M. Desrochers, Y. Zhou, and J.E. LeDoux Two different lateral amygdala cell populations contribute to the initiation and storage of memory Nat. Neurosci. 4 2001 724 731
51. R.A. Rescorla Behavioral studies of Pavlovian conditioning Annu. Rev. Neurosci. 11 1988 329 352
52. M.T. Rogan, U.V. Stäubli, and J.E. LeDoux Fear conditioning induces associative long-term potentiation in the amygdala Nature 390 1997 604 607
53. L.M. Romanski, M.C. Clugnet, F. Bordi, and J.E. LeDoux Somatosensory and auditory convergence in the lateral nucleus of the amygdala Behav. Neurosci. 107 1993 444 450
54. J.B. Rosen The neurobiology of conditioned and unconditioned fear: a neurobehavioral system analysis of the amygdala Behav. Cogn. Neurosci. Rev. 3 2004 23 41
55. J.A. Rosenkranz, and A.A. Grace Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning Nature 417 2002 282 287
56. F.T. Russchen, I. Bakst, D.G. Amaral, and J.L. Price The amygdalostriatal projections in the monkey. An anterograde tracing study Brain Res. 329 1985 241 257
57. P. Sah, E.S. Faber, M. Lopez De Armentia, and J. Power The amygdaloid complex: anatomy and physiology Physiol. Rev. 83 2003 803 834
58. P. Sah, R.F. Westbrook, and A. Lüthi Fear conditioning and long-term potentiation in the amygdala: what really is the connection? Ann. N Y Acad. Sci. 1129 2008 88 95
59. C.D. Salzman, and S. Fusi Emotion, cognition, and mental state representation in amygdala and prefrontal cortex Annu. Rev. Neurosci. 33 2010 173 202
60. M. Sarter, and H.J. Markowitsch Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations Behav. Neurosci. 99 1985 342 380
61. G. Schoenbaum, A.A. Chiba, and M. Gallagher Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning Nat. Neurosci. 1 1998 155 159
62. W. Schultz Reward signaling by dopamine neurons Neuroscientist 7 2001 293 302
63. W. Schultz Behavioral theories and the neurophysiology of reward Annu. Rev. Psychol. 57 2006 87 115
64. K. Schwabe, U. Ebert, and W. Löscher The central piriform cortex: anatomical connections and anticonvulsant effect of GABA elevation in the kindling model Neuroscience 126 2004 727 741
65. B. Seymour, and R. Dolan Emotion, decision making, and the amygdala Neuron 58 2008 662 671
66. S.J. Shabel, and P.H. Janak Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal Proc. Natl. Acad. Sci. USA 106 2009 15031 15036
67. D.D. Stettler, and R. Axel Representations of odor in the piriform cortex Neuron 63 2009 854 864
68. G.D. Stuber, D.R. Sparta, A.M. Stamatakis, W.A. van Leeuwen, J.E. Hardjoprajitno, S. Cho, K.M. Tye, K.A. Kempadoo, F. Zhang, K. Deisseroth, and A. Bonci Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking Nature 475 2011 377 380
69. K.M. Tye, G.D. Stuber, B. de Ridder, A. Bonci, and P.H. Janak Rapid strengthening of thalamo-amygdala synapses mediates cue-reward learning Nature 453 2008 1253 1257
70. K.M. Tye, R. Prakash, S.Y. Kim, L.E. Fenno, L. Grosenick, H. Zarabi, K.R. Thompson, V. Gradinaru, C. Ramakrishnan, and K. Deisseroth Amygdala circuitry mediating reversible and bidirectional control of anxiety Nature 471 2011 358 362
71. T. Uwano, H. Nishijo, T. Ono, and R. Tamura Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala Neuroscience 68 1995 339 361
72. S.B. Wolff, J. Gründemann, P. Tovote, S. Krabbe, G.A. Jacobson, C. Müller, C. Herry, I. Ehrlich, R.W. Friedrich, J.J. Letzkus, and A. Lüthi Amygdala interneuron subtypes control fear learning through disinhibition Nature 509 2014 453 458
73. A.P. Yiu, V. Marcaldo, C. Yan, B. Richards, H.L. Hsiang, J. Pressey, V. Mahadevan, M.M. Tran, S.A. Kushner, and M.A. Woodin Neurons are recruited to a memory trace based on relative excitability immediately before training Neuron 83 2014 722 735
74. F. Zhang, V. Gradinaru, A.R. Adamantidis, R. Durand, R.D. Airan, L. de Lecea, and K. Deisseroth Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures Nat. Protoc. 5 2010 439 456