Neurobiological mechanisms underlying the blocking effect in aversive learning

Journal of Neuroscience

Volumn 32, Issue 38, 2012, Pages 13164-13176

  Eippert, Falk ^a   Gamer, Matthias ^a   Büchel, Christian ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; ATTENTION; AVERSION; BEHAVIOR; CONDITIONING; ELECTROSTIMULATION; EYE TRACKING; FEAR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NORMAL HUMAN; PRIORITY JOURNAL; REINFORCEMENT; RESPONSE TIME; STIMULUS RESPONSE; VENTROMEDIAL PREFRONTAL CORTEX; VISUAL STIMULATION;

EID: 84866389456     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1210-12.2012     Document Type: Article

References (92)

1. Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR (2005) A mechanism for impaired fear recognition after amygdala damage. Nature 433:68-72.
2. Anderson AK, Phelps EA (2001) Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411:305-309.
3. Bach DR, Weiskopf N, Dolan RJ (2011) A stable sparse fear memory trace in human amygdala. J Neurosci 31:9383-9389.
4. Beckers T, De Houwer J, Pineño O, Miller RR (2005) Outcome additivity and outcome maximality influence cue competition in human causal learning. J Exp Psychol Learn Mem Cogn 31:238-249.
5. Beckers T, Miller RR, De Houwer J, Urushihara K (2006) Reasoning rats: forward blocking in Pavlovian animal conditioning is sensitive to constraints of causal inference. J Exp Psychol Gen 135:92-102.
6. Beesley T, Le Pelley ME (2011) The influence of blocking on overt attention and associability in human learning. J Exp Psychol Anim Behav Process 37:114-120.
7. Belova MA, Paton JJ, Morrison SE, Salzman CD (2007) Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron 55:970-984.
8. Bermudez MA, Schultz W (2010) Responses of amygdala neurons to positive reward-predicting stimuli depend on background reward (contingency) rather than stimulus-reward pairing (contiguity). J Neurophysiol 103:1158-1170.
9. Buchel C, Morris J, Dolan RJ, Friston KJ (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20:947-957.
10. Carter RM, O'Doherty JP, Seymour B, Koch C, Dolan RJ (2006) Contingency awareness in human aversive conditioning involves the middle frontal gyrus. Neuroimage 29:1007-1012.
11. Crowne DP, Marlowe D (1960) A new scale of social desirability independent of psychopathology. J Consult Psychol 24:349-354.
12. Davey GC, Singh J (1988) The Kamin "blocking" effect and electrodermal conditioning in humans. J Psychophysiol 2:17-25.
13. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13-34.
14. Dawson ME, Schell AM, Filion DL (2007) The electrodermal system. In: Handbook of psychophysiology (Cacioppo JT, Tassinary LG, Berntson GG, eds), pp 159-182. Cambridge, UK: Cambridge UP.
15. Deckers RH, van Gelderen P, Ries M, Barret O, Duyn JH, Ikonomidou VN, Fukunaga M, Glover GH, de Zwart JA (2006) An adaptive filter for suppression of cardiac and respiratory noise in MRI time series data. Neuroimage 33:1072-1081.
16. Deichmann R, Gottfried JA, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19:430-441.
17. Delgado MR, Nearing KI, Ledoux JE, Phelps EA (2008a) Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron 59:829-838.
18. Delgado MR, Li J, Schiller D, Phelps EA (2008b) The role of the striatum in aversive learning and aversive prediction errors. Philos Trans R Soc Lond B Biol Sci 363:3787-3800.
19. Dickinson A, Shanks D, Evenden J (1984) Judgement of act-outcome contingency: the role of selective attribution. Q J Exp Psychol A 36:29-50.
20. Egger MD, Miller NE (1962) Secondary reinforcement in rats as a function of information value and reliability of the stimulus. J Exp Psychol 64:97-104.
21. Eippert F, Bingel U, Schoell ED, Yacubian J, Klinger R, Lorenz J, Buchel C (2009) Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 63:533-543.
22. Fanselow MS (1998) Pavlovian conditioning, negative feedback, and blocking: mechanisms that regulate association formation. Neuron 20:625-627.
23. Fletcher PC, Anderson JM, Shanks DR, Honey R, Carpenter TA, Donovan T, Papadakis N, Bullmore ET (2001) Responses of human frontal cortex to surprising events are predicted by formal associative learning theory. Nat Neurosci 4:1043-1048.
24. Fredrikson M (1981) Orienting and defensive reactions to phobic and conditioned fear stimuli in phobics and normals. Psychophysiology 18: 456-465.
25. Freese JL, Amaral DG (2009) Neuroanatomy of the primate amygdala. In: The human amygdala (Whalen PJ, Phelps EA, eds), pp 3-42. New York: Guilford Press.
26. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218-229.
27. Gamer M, Buchel C (2009) Amygdala activation predicts gaze toward fearful eyes. J Neurosci 29:9123-9126.
28. Gamer M, Zurowski B, Buchel C (2010) Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc Natl Acad Sci U S A 107:9400-9405.
29. Gläscher J (2009) Visualization of group inference data in functional neuroimaging. Neuroinformatics 7:73-82.
30. Gläscher J, Buchel C (2005) Formal learning theory dissociates brain regions with different temporal integration. Neuron 47:295-306.
31. Gläscher J, Daw N, Dayan P, O'Doherty JP (2010) States versus rewards: dissociable neural prediction error signals underlying model-based and model-free reinforcement learning. Neuron 66:585-595.
32. Glautier S (2002) Spatial separation of target and competitor cues enhances blocking of human causality judgements. Q J Exp Psychol B 55:121-135.
33. Hamm AO, Vaitl D (1996) Affective learning: awareness and aversion. Psychophysiology 33:698-710.
34. Hare RD, Blevings G (1975) Conditioned orienting and defensive responses. Psychophysiology 12:289-297.
35. Haselgrove M (2010) Reasoning rats or associative animals? A commonelement analysis of the effects of additive and subadditive pretraining on blocking. J Exp Psychol Anim Behav Process 36:296-306.
36. Hinchy J, Lovibond PF, Ter-Horst KM (1995) Blocking in human electrodermal conditioning. Q J Exp Psychol B 48:2-12.
37. Hodes RL, Cook EW 3rd, Lang PJ (1985) Individual differences in autonomic response: conditioned association or conditioned fear? Psycho-physiology 22:545-560.
38. Hogarth L, Dickinson A, Duka T (2010) Selective attention to conditioned stimuli in human discrimination learning: untangling the effects of outcome prediction, valence, arousal, and uncertainty. In: Attention and associative learning (Mitchell CJ, Le Pelley ME, eds), pp 71-98. Oxford, UK: Oxford UP.
39. Holland PC, Gallagher M (1999) Amygdala circuitry in attentional and representational processes. Trends Cogn Sci 3:65-73.
40. Holland PC, Han JS, Gallagher M (2000) Lesions of the amygdala central nucleus alter performance on a selective attention task. J Neurosci 20:6701-6706.
41. Iordanova MD (2010) Dopamine transmission in the amygdala modulates surprise in an aversive blocking paradigm. Behav Neurosci 124:780-788.
42. Iordanova MD, McNally GP, Westbrook RF (2006) Opioid receptors in the nucleus accumbens regulate attentional learning in the blocking paradigm. J Neurosci 26:4036-4045.
43. Johansen JP, Cain CK, Ostroff LE, LeDoux JE (2011) Molecular mechanisms of fear learning and memory. Cell 147:509-524.
44. Kamin LJ (1968) "Attention-like" processes in classical conditioning. In: Miami symposium on the prediction of behavior, 1967: aversive stimulation (Jones MR, ed), pp 9-31. Coral Gables. FL: University of Miami.
45. Kim JJ, Krupa DJ, Thompson RF (1998) Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279: 570-573.
46. Klinge C, Röder B, Buchel C (2010) Increased amygdala activation to emotional auditory stimuli in the blind. Brain 133:1729-1736.
47. Kluge C, Bauer M, Leff AP, Heinze HJ, Dolan RJ, Driver J (2011) Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal. Proc Natl Acad Sci U S A 108:12545-12550.
48. Klumpers F, Raemaekers MA, Ruigrok AN, Hermans EJ, Kenemans JL, Baas JM (2010) Prefrontal mechanisms of fear reduction after threat offset. Biol Psychiatry 68:1031-1038.
49. Kruschke JK, Kappenman ES, Hetrick WP (2005) Eye gaze and individual differences consistent with learned attention in associative blocking and highlighting. J Exp Psychol Learn Mem Cogn 31:830-845.
50. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA (1998) Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20:937-945.
51. Li J, Schiller D, Schoenbaum G, Phelps EA, Daw ND (2011) Differential roles of human striatum and amygdala in associative learning. Nat Neurosci 14:1250-1252.
52. Livesey EJ, Boakes RA (2004) Outcome additivity, elemental processing and blocking in human causality judgements. Q J Exp Psychol B 57:361-379.
53. Lovibond PF, Siddle DA, Bond N (1988) Insensitivity to stimulus validity in human pavlovian conditioning. Q J Exp Psychol B 40:377-410.
54. Luck HE, Timaeus E (1969) Scales for the measurement of manifest anxiety (MAS) and social desirability (SDS-E and SDS-CM). Diagnostica 15:134-141.
55. Mackintosh NJ (1975) A theory of attention: variations in the associability of stimuli with reinforcement. Psychol Rev 82:276-298.
56. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852.
57. Martin I, Levey AB (1991) Blocking observed in human eyelid conditioning. QJExpPsycholB43:233-256.
58. McNally GP, Cole S (2006) Opioid receptors in the midbrain periaqueductal gray regulate prediction errors during pavlovian fear conditioning. Behav Neurosci 120:313-323.
59. McNally GP, Pigg M, Weidemann G (2004) Blocking, unblocking, and overexpectation of fear: a role for opioid receptors in the regulation of Pavlovian association formation. Behav Neurosci 118:111-120.
60. McNally GP, Johansen JP, Blair HT (2011) Placing prediction into the fear circuit. Trends Neurosci 34:283-292.
61. Mechias ML, Etkin A, Kalisch R (2010) A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. Neuroimage 49:1760-1768.
62. Melchers KG, Shanks DR, Lachnit H (2008) Stimulus coding in human associative learning: flexible representations of parts and wholes. Behav Processes 77:413-427.
63. Mitchell CJ, Lovibond PF (2002) Backward and forward blocking in human electrodermal conditioning: blocking requires an assumption of outcome additivity. Q J Exp Psychol B 55:311-329.
64. Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653-660.
65. Nili U, Goldberg H, Weizman A, Dudai Y (2010) Fear thou not: activity of frontal and temporal circuits in moments of real-life courage. Neuron 66:949-962.
66. Ohman A (2009) Human fear conditioning and the amygdala. In: The human amygdala (Whalen PJ, Phelps EA, eds), pp 118-154. New York: Guilford Press.
67. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439:865-870.
68. Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. London: Oxford UP.
69. Pearce JM, Hall G (1980) A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol Rev 87:532-552.
70. Phelps EA (2009) The human amygdala and the control of fear. In: The human amygdala (Whalen PJ, Phelps EA, eds), pp 204-219. New York: Guilford Press.
71. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897-905.
72. Prados J (2011) Blocking and overshadowing in human geometry learning. J Exp Psychol Anim Behav Process 37:121-126.
73. Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15:1029-1039.
74. Reinhard G, Lachnit H (2002) Differential conditioning of anticipatory pupillary dilation responses in humans. Biol Psychol 60:51-68.
75. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4:724-731.
76. Rescorla RA (1981) Within-signal learning in autoshaping. Anim Learn Behav 9:245-252.
77. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Classical conditioning II: current research and theory (Black AH, Prokasy WF, eds), pp 64-99. New York: Appleton-Century-Crofts.
78. Rosenkranz JA, Moore H, Grace AA (2003) The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci 23:11054-11064.
79. Salvucci DD, Goldberg JH (2000) Identifying fixations and saccades in eyetracking protocols. In: Proceedings of the 2000 Symposium on Eye Tracking Research and Applications, pp 71-78. New York: ACM.
80. Sander D, Grafman J, Zalla T (2003) The human amygdala: an evolved system for relevance detection. Rev Neurosci 14:303-316.
81. Schiller D, Levy I, Niv Y, LeDoux JE, Phelps EA (2008) From fear to safety and back: reversal of fear in the human brain. J Neurosci 28:11517-11525.
82. Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4:e5865.
83. Shanks DR (2010) Learning: from association to cognition. Annu Rev Psychol 61:273-301.
84. Spielberger C, Gorsuch R, Lushene R, Vagg P, Jacobs G (1970) State-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press.
85. Stephan KE, Friston KJ (2010) Analyzing effective connectivity with fMRI. Wiley Interdiscip Rev Cogn Sci 1:446-459.
86. Tobler PN, O'doherty JP, Dolan RJ, Schultz W (2006) Human neural learning depends on reward prediction errors in the blocking paradigm. J Neurophysiol 95:301-310.
87. Turner DC, Aitken MR, Shanks DR, Sahakian BJ, Robbins TW, Schwarzbauer C, Fletcher PC (2004) The role of the lateral frontal cortex in causal associative learning: exploring preventative and super-learning. Cereb Cortex 14:872-880.
88. Vandorpe S, De Houwer J (2005) A comparison of forward blocking and reduced overshadowing in human causal learning. Psychon Bull Rev 12:945-949.
89. Velden M, Wölk C (1987) Depicting cardiac activity over real time: a proposal for standardization. J Psychophysiol 1:173-175.
90. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728-733.
91. Waelti P, Dickinson A, Schultz W (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature 412:43-48.
92. Wills AJ, Lavric A, Croft GS, Hodgson TL (2007) Predictive learning, prediction errors, and attention: evidence from event-related potentials and eye tracking. J Cogn Neurosci 19:843-854.