The basolateral amygdala is necessary for negative prediction errors to enhance cue salience, but not to produce conditioned inhibition

European Journal of Neuroscience

Volumn 40, Issue 9, 2014, Pages 3328-3337

  Esber, Guillem R ^a   Holland, Peter C ^b  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Associative learning; Basolateral amygdala; Conditioned inhibition; Prediction error; Salience; Unblocking

Indexed keywords

PROTEIN FOS; PROTEIN C FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BEHAVIORAL SCIENCE; BRAIN CELL; BRAIN HISTOLOGY; COGNITION; CONDITIONED INHIBITION; CONDITIONING; CONTROLLED STUDY; ERROR; INHIBITION (PSYCHOLOGY); MALE; NEGATIVE PREDICTION ERROR; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REINFORCEMENT; SALIENCE; ANIMAL; ASSOCIATION; ATTENTION; CONDITIONED REFLEX; LONG EVANS RAT; METABOLISM; PHYSIOLOGY;

ANIMALS; ATTENTION; BASOLATERAL NUCLEAR COMPLEX; CONDITIONING, CLASSICAL; CUES; INHIBITION (PSYCHOLOGY); MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS, LONG-EVANS;

EID: 84932116166     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12695     Document Type: Article

References (36)

1. Belova, M.A., Paton, J.J., Morrison, S.E. & Salzman, C.D. (2007) Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron, 55, 970-984.
2. Bucci, D.J., Holland, P.C. & Gallagher, M. (1998) Removal of cholinergic input to rat posterior parietal cortex disrupts incremental processing of conditioned stimuli. J. Neurosci., 18, 8038-8046.
3. Calu, D.J., Roesch, M.R., Haney, R.Z., Holland, P.C. & Schoenbaum, G. (2010) Neural correlates of variations in event processing during learning in central nucleus of amygdala. Neuron, 68, 991-1001.
4. Chang, S.E., McDannald, M.A., Wheeler, D.S. & Holland, P.C. (2012) The effects of basolateral amygdala lesions on unblocking. Behav. Neurosci., 126, 279-289.
5. Chiba, A.A., Bucci, D.J., Holland, P.C. & Gallagher, M. (1995) Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J. Neurosci., 15, 7315-7322.
6. Denniston, J.C., Cole, R.P. & Miller, R.R. (1998) The role of temporal relationships in the transfer of conditioned inhibition. J. Exp. Psychol. Anim. B., 24, 200-214.
7. Dickinson, A., Hall, G. & Mackintosh, N.J. (1976) Surprise and the attenuation of blocking. J. Exp. Psychol. Anim. B., 2, 313-322.
8. Esber, G.R., Roesch, M.R., Bali, S., Trageser, J., Bissonette, G.B., Puche, A.C., Holland, P.C. & Schoenbaum, G. (2012) Attention-related Pearce-Kaye-Hall signals in basolateral amygdala require the midbrain dopaminergic system. Biol. Psychiat., 72, 1012-1019.
9. Hall, G. & Pearce, J.M. (1982) Restoring the associability of a preexposed CS by a surprising event. Q. J. Exp. Psychol., 34B, 127-140.
10. Hatfield, T., Han, J.S., 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.
11. Holland, P.C. (1988) Excitation and inhibition in unblocking. J. Exp. Psychol. Anim. B., 14, 261-279.
12. Holland, P.C. (2006) Enhanced conditioning produced by surprising increases in reinforcer value are unaffected by lesions of the amygdala central nucleus. Neurobiol. Learn. Mem., 85, 30-35.
13. Holland, P.C. (2012) Role of amygdala central nucleus in feature negative discriminations. Behav. Neurosci., 126, 670-680.
14. Holland, P.C. & Gallagher, M. (1993a) Amygdala central nucleus lesions disrupt increments, but not decrements, in conditioned stimulus processing. Behav. Neurosci., 107, 246-253.
15. Holland, P.C. & Gallagher, M. (1993b) Effects of amygdala central nucleus lesions on blocking and unblocking. Behav. Neurosci., 107, 235-245.
16. Holland, P.C. & Kenmuir, C. (2005) Variations in unconditioned stimulus processing in unblocking. J. Exp. Psychol. Anim. B., 31, 155-171.
17. Holland, P.C. & Maddux, J.-M. (2010) Brain systems of attention in associative learning. In Mitchell, C.J. & LePelley, M.E. (Eds), Attention and Learning. Oxford University Press, Oxford, pp. 305-349.
18. Holland, P.C., Thornton, J.A. & Ciali, L. (2000) The influence of associability changes in negative patterning and other discriminations. J. Exp. Psychol. Anim. B., 26, 462-476.
19. Holland, P.C., Chik, Y. & Zhang, Q. (2001a) Inhibitory learning tests of conditioned stimulus associability in rats with lesions of the amygdala central nucleus. Behav. Neurosci., 115, 1154-1158.
20. Holland, P.C., Hatfield, T. & Gallagher, M. (2001b) Rats with basolateral amygdala lesions show normal increases in conditioned stimulus processing but reduced conditioned potentiation of eating. Behav. Neurosci., 115, 945-950.
21. Kamin, L.J. (1969) Selective association and conditioning. In Mackintosh, N.J. & Honig, W.K. (Eds), Fundamental Issues in Associative Learning. Dalhousie University Press, Halifax, pp. 42-64.
22. Lee, H.J., Groshek, F., Petrovich, G.D., Cantalini, J.P., Gallagher, M. & Holland, P.C. (2005) Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J. Neurosci., 25, 3881-3888.
23. Lee, H.J., Youn, J.M., Gallagher, M. & Holland, P.C. (2008) Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning. Eur. J. Neurosci., 27, 3043-3049.
24. LePelley, M.E. (2004) The role of associative history in models of associative learning: a selective review and a hybrid model. Q. J. Exp. Psychol., 57, 193-243.
25. Mackintosh, N.J. & Cotton, M.M. (1985) Conditioned inhibition from reinforcement reduction. In Miller, R.R. & Spear, N.E. (Eds), Information Processing in Animals: Conditioned Inhibition. Erlbaum, Hillsdale, NJ, pp. 89-111.
26. Matzel, L.D., Gladstein, L. & Miller, R.R. (1988) Conditioned excitation and conditioned inhibition are not mutually exclusive. Learn. Motiv., 19, 99-121.
27. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
28. Pearce, J.M. & Hall, G. (1980) A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev., 87, 532-552.
29. Pearce, J.M. & Mackintosh, N.J. (2010) Two theories of attention: a review and a possible integration. In Mitchell, C.J. & LePelley, M.E. (Eds), Attention and Associative Learning: From Brain to Behaviour. Oxford University Press, Oxford, UK, pp. 11-39.
30. Pearce, J.M., Kaye, H. & Hall, G. (1982) Predictive accuracy and stimulus associability: development of a model for Pavlovian learning. In Commons, M.L., Herrnstein, R.J. & Wagner, A.R. (Eds), Quantitative Analyses of Behavior. Ballinger, Cambridge, MA, pp. 241-255.
31. Pearce, J.M., George, D.N. & Redhead, E.S. (1998) The role of attention in the solution of conditional discriminations. In Schmajuk, N.A. & Holland, P.C. (Eds), Occasion Setting: Associative Learning and Cognition in Animals. APA Press, Washington, DC, pp. 249-275.
32. Rescorla, R.A. & Wagner, A.R. (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In Black, A.H. & Prokesy, W.F. (Eds), Classical Conditioning II: Current Research and Theory. Appleton Century Crofts, New York, pp. 64-99.
33. Roesch, M.R., Calu, D.J., Esber, G.R. & Schoenbaum, G. (2010) Neural correlates of variations in event processing during learning in basolateral amygdala. J. Neurosci., 30, 2464-2471.
34. Schiffino, F.L., Zhou, V. & Holland, P.C. (2014) Posterior parietal cortex is critical for the encoding, consolidation, and retrieval of a memory that guides attention for learning. Eur. J. Neurosci., 39, 640-649.
35. Schultz, W. & Dickinson, A. (2000) Neuronal coding of prediction errors. Annu. Rev. Neurosci., 23, 473-500.
36. Wagner, A.R., Mazur, J.E., Donegan, N.H. & Pfautz, P.L. (1980) Evaluation of blocking and conditioned inhibition to a CS signaling a decrease in US intensity. J. Exp. Psychol. Anim. B., 6, 376-385.