Role of amygdala central nucleus in aversive learning produced by shock or by unexpected omission of food

Journal of Neuroscience

Volumn 32, Issue 7, 2012, Pages 2461-2472

  Purgert, Robert J ^a   Wheeler, Daniel S ^a   Mcdannald, Michael A ^a   Holland, Peter C ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARC PROTEIN; MESSENGER RNA; PROTEIN; PROTEIN HOMER 1A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APPETITE; ARTICLE; AVERSIVE BEHAVIOR; BEHAVIOR; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; FOOD AVERSION; GENE EXPRESSION; HISTOLOGY; IMMEDIATE EARLY GENE; LIGHT EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; PUNISHMENT; RAT; REINFORCEMENT; REWARD; SHOCK; STIMULUS;

AMYGDALA; ANIMALS; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); ELECTROSHOCK; FOOD DEPRIVATION; MALE; NEURONS; RATS; RATS, LONG-EVANS; REWARD; TIME FACTORS;

EID: 84857074979     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5090-11.2012     Document Type: Article

References (44)

1. Amsel A (1958) The role of frustrative nonreward in noncontinuous reward situations. Psychol Bull 55:102-119.
2. Balleine BW (2005) Neural bases of food-seeking: affect, arousal and rewards in corticostraitolimbic circuits. Physiol Behav 86:717-730.
3. Berridge KC (2001) Reward learning: reinforcement, incentives, and expectations. Psychol Learn Motiv 40:223-278.
4. Bolles RC (1972) Reinforcement, expectancy, and learning. Psychol Rev 79:394-409.
5. Bottai D, Guzowski JF, Schwarz MK, Kang SH, Xiao B, Lanahan A, Worley PF, Seeburg PH (2002) Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J Neurosci 22:167-175.
6. Calu DJ, Roesch MR, Haney RZ, Holland PC, Schoenbaum G (2010) Neural correlates of variations in event processing during learning in central nucleus of amygdala. Neuron 68:991-1001.
7. Choi JS, Cain CK, LeDoux JE (2010) The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem 17:139-147.
8. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Müller C, Lüthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277-282.
9. Corbit LH, Balleine BW (2005) The general and outcome-specific forms of Pavlovian-instrumental transfer are differentially mediated by the nucleus accumbens core and shell. J Neurosci 25:962-970.
10. Corbit LH, Balleine BW (2011) Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of Pavlovian-instrumental transfer. J Neurosci 31:11786-11794.
11. Davis M (2000) The role of the amygdala in conditioned and unconditioned fear and anxiety. In: The amygdala: a functional analysis (Aggleton JP, ed), pp 213-287. Oxford: Oxford UP.
12. Dickinson A, Dearing MF (1979) Appetitive aversive interactions and inhibitory processes. In: Mechanisms of learning and motivation (Dickinson A, Boakes RA, eds), pp 203-231. Hillsdale, NJ: Erlbaum.
13. Estes KW, Skinner BF (1941) Some quantitative properties of anxiety. J Exp Psychol 29:390-400.
14. Gewirtz JC, Davis M (1997) Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Nature 388:471-474.
15. Hatfield T, Han JS, Conley M, Gallagher M, Holland P (1996) Neurotoxic lesions of basolateral, but not central amygdala interfere with Pavlovian second-order conditioning and reinforcer-devaluation effects. J Neurosci 16:5256-5265.
16. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R, Biag J, Dong HW, Deisseroth K, Callaway EM, Fanselow MS, Lüthi A, Anderson DJ (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468:270-276.
17. Holland PC (1980) Second-order conditioning with and without unconditioned stimulus presentation. J Exp Psychol Anim Behav Proc 6:238-250.
18. Holland PC, Gallagher M (1993a) Amygdala central nucleus lesions disrupt increments, but not decrements, in conditioned stimulus processing. Behav Neurosci 107:246-253.
19. Holland PC, Gallagher M (1993b) Effects of amygdala central nucleus lesions on blocking and unblocking. Behav Neurosci 107:235-245.
20. Holland PC, Gallagher M (1999) Amygdala circuitry in attentional and representational processes. Trends Cogn Sci 3:65-73.
21. Holland PC, Maddux JM (2010) Brain systems of attention in associative learning. In: Attention and learning (Mitchell CJ, LePelley ME, eds), pp 305-349. Oxford: Oxford UP.
22. Holland PC, Chik Y, Zhang Q (2001) Inhibitory learning tests of condi-tioned stimulus associability in rats with lesions of the amygdala central nucleus. Behav Neurosci 115:1154-1158.
23. Kemble ED, Beckman GJ (1970) Runway performance of rats following amygdaloid lesions. Physiol Behav 5:45-47.
24. Killcross S, Robbins TW, Everitt BJ (1997) Different types of fear conditioned behavior mediated by separate nuclei within amygdala. Nature 388:377-380.
25. Koo JW, Han JS, Kim JJ (2004) Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci 24:7654-7662.
26. LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727-738.
27. Lee HJ, Groshek F, Petrovich GD, Cantalini JP, Gallagher M, Holland PC (2005) Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J Neurosci 25:3881-3888.
28. Lee HJ, Gallagher M, Holland PC (2010) The central amygdala projection to the substantia nigra reflects prediction error information in appetitive conditioning. Learn Mem 17:531-538.
29. Lee JL, Dickinson A, Everitt BJ (2005) Conditioned suppression and freezing as measures of aversive Pavlovian conditioning: effects of discrete amygdala lesions and overtraining. Behav Brain Res 159:221-233.
30. Lolordo VM (1969) Positive conditioned reinforcement from aversive situations. Psychol Bull 72:193-203.
31. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeletonassociated protein that is enriched in neuronal dendrites. Neuron 14:433-445.
32. Mahler SV, Berridge KC (2009) Which cue to "want?" Central amygdala opioid activation enhances and focuses incentive salience on a prepotent reward cue. J Neurosci 29:6500-6513.
33. McDannald MA (2010) Contributions of the amygdala central nucleus and ventrolateral periaqueductal grey to freezing and instrumental suppression in Pavlovian fear conditioning. Behav Brain Res 211:111-117.
34. Mowrer OH (1947) On the dual nature of learning: a reinterpretation of conditioning and problem solving. Harv Educ Rev 17:102-148.
35. Mowrer OH (1960) Learning theory and behavior. New York: Wiley.
36. Pearce JM, Hall G (1980) A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol Rev 106:532-552.
37. Petrovich GD, Holland PC, Gallagher M (2005) Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J Neurosci 25:8295-8302.
38. Petrovich GD, Ross CA, Mody P, Holland PC, Gallagher M (2009) Central, but not basolateral amygdala, is critical for control of feeding by aversive learned cues. J Neurosci 29:15205-15212.
39. Rescorla RA (2003) Protection from extinction. Learn Behav 31:124-132.
40. Rescorla RA, Solomon RL (1967) Two process learning theory: relationships between classical conditioning and instrumental learning. Psychol Rev 74:151-182.
41. Rescorla RA Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Classical conditioning II (Black AH, Prokasy WF, eds), pp 64-99. New York: Appleton Century Crofts.
42. Saddoris MP, Holland PC, Gallagher M (2009) Associatively-learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex. J Neurosci 29:15386-15396.
43. Swanson LW (1998) Brain maps: Computer graphics files. Amsterdam: Elsevier.
44. Vazdarjanova A, Guzowski JF (2004) 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.