The birth, death and resurrection of avoidance: A reconceptualization of a troubled paradigm

Molecular Psychiatry

Volumn 22, Issue 1, 2017, Pages 24-36

  LeDoux, J E ^a,b   Moscarello, J ^a   Sears, R ^a   Campese, V ^a  

^a NEW YORK UNIVERSITY   (United States)

^b NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVOIDANCE BEHAVIOR; BEHAVIOR CHANGE; BEHAVIOR CONTROL; CONDITIONING; CONNECTOME; ESCAPE BEHAVIOR; FEAR; HUMAN; LEARNING; NONHUMAN; PAVLOVIAN THREAT CONDITIONING; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; ANIMAL; ANXIETY; CONDITIONED REFLEX; INSTRUMENTAL CONDITIONING; PHYSIOLOGY; PSYCHOLOGY; THERAPY;

ANIMALS; ANXIETY; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; FEAR; HUMANS; REINFORCEMENT (PSYCHOLOGY);

EID: 84991677958     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.166     Document Type: Review

References (233)

1. Marks I. Fears, Phobias, and Rituals: Panic, Anxiety and Their Disorders. Oxford University Press: New York, NY, USA, 1987.
2. Barlow DH. Anxiety and Its Disorders: The Nature and Treatment of Anxiety and Panic. Guilford Press: New York, NY, USA, 2002.
3. Lazarus RS. Psychological Stress and the Coping Process. McGraw Hill: New York, NY, USA, 1966.
4. Holahan CJ, Moos RH. Risk, resistance, and psychological distress: a longitudinal analysis with adults and children. J Abnorm Psychol 1987; 96: 3-13.
5. Foa EB, Kozak MJ. Emotional processing of fear: exposure to corrective information. Psychol Bull 1986; 99: 20-35.
6. Mineka S. The role of fear in theories of avoidance learning, flooding, and extinction. Psychol Bull 1979; 86: 985-1010.
7. Rachman S. Anxiety2nd ednPsychology Press: Hove, England, 2004.
8. Hofmann SG. Emotion in Therapy: From Science to Practice. Guilford Press: New York, NY, USA, 2016.
9. Mowrer OH. A stimulus-response analysis of anxiety and its role as a reinforcing agent. Psychol Rev 1939; 46: 553-565.
10. Mowrer OH. Learning Theory and Behavior. Wiley: New York, NY, USA, 1960.
11. Mowrer OH. Anxiety-reduction and learning. J Exp Psychol 1940; 27: 497-516.
12. Kapp BS, Pascoe JP, Bixler MA. The amygdala: a neuroanatomical systems approach to its contributions to aversive conditioning. In: Buttlers N, Squire LR (eds). Neuropsychology of Memory. Guilford: New York, NY, USA, 1984 pp 473-488.
13. LeDoux JE, Sakaguchi A, Reis DJ. Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci 1984; 4: 683-698.
14. Hitchcock J, Davis M. Lesions of the amygdala but not of the cerebellum or red nucleus block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986; 100: 11-22.
15. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000; 23: 155-184.
16. Johansen JP, Cain CK, Ostroff LE, LeDoux JE. Molecular mechanisms of fear learning and memory. Cell 2011; 147: 509-524.
17. Duvarci S, Pare D. Amygdala microcircuits controlling learned fear. Neuron 2014; 82: 966-980.
18. Pape HC, Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 2010; 90: 419-463.
19. Fanselow MS, Poulos AM. The neuroscience of mammalian associative learning. Annu Rev Psychol 2005; 56: 207-234.
20. Tovote P, Fadok JP, Luthi A. Neuronal circuits for fear and anxiety. Nat Rev Neurosci 2015; 16: 317-331.
21. Rosen JB, Schulkin J. From normal fear to pathological anxiety. Psychol Rev 1998; 105: 325-350.
22. LeDoux JE. Synaptic Self: How Our Brains Become Who We Are. Viking: New York, NY, USA, 2002.
23. Cain C, LeDoux JE. Emotional processing and motivation: in search of brain mechanisms. In: Elliot AJ(ed). Handbook of Approach and Avoidance Motivation. Psychology Press, Taylor and Francis Group, LLC: New York, NY, USA, 2008 pp 17-34.
24. LeDoux JE, Schiller D, Cain C. Emotional reaction and action: from threat processing to goal-directed behavior. In: Gazzaniga MS(ed). The Cognitive Neurosciences, 4th edn. MIT Press: Cambridge, MA, USA, 2009 pp 905-924.
25. Krypotos AM, Effting M, Kindt M, Beckers T. Avoidance learning: a review of theoretical models and recent developments. Front Behav Neurosci 2015; 9: 189.
26. Servatius RJ. Editorial: avoidance: from basic science to psychopathology. Front Behav Neurosci 2016; 10: 15.
27. Oleson EB, Gentry RN, Chioma VC, Cheer JF. Subsecond dopamine release in the nucleus accumbens predicts conditioned punishment and its successful avoidance. J Neurosci 2012; 32: 14804-14808.
28. Campese VD, Sears RM, Moscarello JM, Diaz-Mataix L, Cain CK, LeDoux JE. The neural foundations of reaction and action in aversive motivation. Curr Top Behav Neurosci 2016; 27: 171-195.
29. Bravo-Rivera C, Roman-Ortiz C, Montesinos-Cartagena M, Quirk GJ. Persistent active avoidance correlates with activity in prelimbic cortex and ventral striatum. Front Behav Neurosci 2015; 9: 184.
30. LeDoux JE. Anxious: Using the Brain to Understand and Treat Fear and Anxiety. Viking: New York, NY, USA, 2015.
31. Herrnstein RJ. Method and theory in the study of avoidance. Psychol Rev 1969; 76: 49-69.
32. Killcross S, Robbins TW, Everitt BJ. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 1997; 388: 377-380.
33. Fernando AB, Urcelay GP, Mar AC, Dickinson A, Robbins TW. Safety signals as instrumental reinforcers during free-operant avoidance. Learn Mem 2014; 21: 488-497.
34. Jiao X, Beck KD, Myers CE, Servatius RJ, Pang KC. Altered activity of the medial prefrontal cortex and amygdala during acquisition and extinction of an active avoidance task. Front Behav Neurosci 2015; 9: 249.
35. Bravo-Rivera C, Roman-Ortiz C, Brignoni-Perez E, Sotres-Bayon F, Quirk GJ. Neural structures mediating expression and extinction of platform-mediated avoidance. J Neurosci 2014; 34: 9736-9742.
36. Watson JB. Behaviorism. W.W. Norton: New York, NY, USA, 1925.
37. Pavlov IP. Conditioned Reflexes. Dover: New York, NY, USA, 1927.
38. Watson JB, Rayner R. Conditioned emotional reactions. J Exp Psychol 1920; 3: 1-14.
39. Skinner BF. The Behavior of Organisms: An Experimental Analysis. Appleton-Cen-tury-Crofts: New York, NY, USA, 1938.
40. Hull CL. Principles of Behavior. Appleton-Century-Crofts: New York, NY, USA, 1943.
41. Tolman EC. Purposive Behavior in Animals and Men. Century: New York, NY, USA, 1932.
42. Freud S. The Problem of Anxiety. W. W. Norton: New York, NY, USA, 1936.
43. Rescorla RA, Solomon RL. Two process learning theory: relationships between Pavlovian conditioning and instrumental learning. Psychol Rev 1967; 74: 151-182.
44. Overmier JB, Brackbill RM. On the independence of stimulus evocation of fear and fear evocation of responses. Behav Res Ther 1977; 15: 51-56.
45. Miller NE. Learnable drives and rewards. In: Stevens SS (ed). Handbook of Experimental Psychology. Wiley: New York, NY, USA, 1951 pp 435-472.
46. Mowrer OH. Two-factor learning theory: summary and comment. Psychol Rev 1951; 58: 350-354.
47. McAllister DE, McAllister WR. Fear theory and aversively motivated behavior: Some controversial issues. In: Denny MR (ed). Fear, Avoidance, and Phobias: A Fundamental Analysis. Erlbaum: Hillsdale, NJ, USA, 1991.
48. McAllister WR, McAllister DE. Behavioral measurement of conditioned fear. In: Brush FR (ed). Aversive Conditioning and Learning. Academic Press: New York, 1971 pp 105-179.
49. Masterson FA, Crawford M. The defense motivation system: a theory of avoidance behavior. Behav Brain Sci 1982; 5: 661-696.
50. Miller NE. Studies of fear as an acquirable drive: I. Fear as motivation and fear reduction as reinforcement in the learning of new responses. J Exp Psychol 1948; 38:89-101.
51. Mowrer OH. On the dual nature of learning: a reinterpretation of "conditioning" and "problem solving". Harvard Educ Rev 1947; 17: 102-148.
52. Levis DJ. The case for a return to a two-factor theory of avoidance: the failure of non-fear interpretations. In: Klein SB, Mowrer RR (eds). Contemporary Learning Theories: Pavlovian Conditioning and the Status of Traditional Learning Theory. Lawrence Erlbaum Assn: Hillsdale, NJ, USA, 1989 pp 227-277.
53. Mowrer OH, Lamoreaux RR. Fear as an intervening variable in avoidance conditioning. J Comp Psych 1946; 39: 29-50.
54. Miller NE. An experimental investigation of acquired drives. Psychol Bull 1941; 38: 534-535.
55. Dinsmoor JA. Punishment. I. The avoidance hypothesis. Psychol Rev 1954; 61: 34-46.
56. Schoenfeld WN. An experimental approach to anxiety, escape, and avoidance behavior. In: Hoch PH, Zubin J (eds). Anxiety. Grune & Stratton: New York, NY, USA, 1950 pp 70-99.
57. Solomon RL, Wynne LC. Traumatic avoidance learning: the principles of anxiety conservation and partial irreversibility. Psychol Rev 1954; 61: 353-385.
58. Kamin LJ. The effects of termination of the CS and avoidance of the US on avoidance learning. J Comp Physiol Psychol 1956; 49: 420-424.
59. Bolles RC. Species-specific defense reactions and avoidance learning. Psychol Rev 1970; 77: 32-48.
60. Bolles RC. The avoidance learning problem. In: Bower GH (ed). The Psychology of Learning and Motivation vol. 6. Academic Press: New York, NY, USA, 1972 pp 97-145.
61. Trapold MA, Overmier JB. The second learning process in instrumental learning. In: Black AA, Prokasy WF (eds). Classical Conditioning 2: Current Research and Theory. Appleton-Century-Crofts: New York, NY, USA, 1972 pp 427-452.
62. Seligman ME, Johnston JC. A cognitive theory of avoidance learning. In: McGuigan FJ, Lumsden DB (eds). Contemporary Approaches to Conditioning and Learning. V. H. Winston & Sons: Oxford, UK, 1973 pp 69-110.
63. Gray JA. The Psychology of Fear and Stress vol. 2. Cambridge University Press: New York, NY, USA, 1971.
64. Overmier JB, Bull JA, Pack K. On instrumental response interaction as explaining the influences of pavlovian cs's upon avoidance behavior. Learn Motiv 1971; 2: 103-112.
65. Riccio DC, Silvestri R. Extinction of avoidance behavior and the problem of residual fear. Behav Res Ther 1973; 11: 1-9.
66. Rescorla RA, LoLordo VM. Inhibition of avoidance behavior. J Comp Physiol Psychol 1965; 59: 406-412.
67. Weiskrantz L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Physiol Psychol 1956; 49: 381-391.
68. Goddard G. Functions of the amygdala. Psychol Rev 1964; 62: 89-109.
69. Grossman SP. A Textbook of Physiological Psychology. John Wiley & Sons, 1967.
70. Thompson R. A Behavioral Atlas of the Rat Brain. Oxford University Press: New York, NY, USA, 1978.
71. Sarter MF, Markowitsch HJ. Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. Behav Neurosci 1985; 99: 342-380.
72. Dollard J, Miller NE. Personality and Psychotherapy: An Analysis in Terms of Learning, Thinking, and Culture. McGraw-Hill: New York, NY, USA, 1950.
73. Stampfl TG, Levis DJ. Essentials of implosive therapy: a learning-theory-based psychodynamic behavioral therapy. J Abnorm Psychol 1967; 72: 496-503.
74. Hofmann SG. Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders. Clin Psychol Rev 2008; 28: 199-210.
75. Dymond S, Roche B. A contemporary behavior analysis of anxiety and avoidance. Behav Anal 2009; 32: 7-27.
76. Gabriel M, Foster K, Orona E, Saltwick SE, Stanton M. Neuronal activity of cingulate cortex, anteroventral thalamus, and hippocampal formation in discriminative conditioning: encoding and extraction of the significance of conditional stimuli. In: Sprague JM, Epstein AN (eds). Progress in Psychobiology and Physiological Psy-chology, vol. 9. Academic Press: New York, NY, USA, 1980 pp 126-232.
77. Fonberg E. The role of the amygdaloid nucleus in animal behaviour. Prog Brain Res 1968; 22: 273-281.
78. Squire L. Memory and Brain. Oxford University Press: New York, NY, USA, 1987.
79. Kandel ER. Cellular Basis of Behavior: An Introduction to Behavioral Neurobiology. W.H. Freeman and Company: San Fransisco, CA, USA, 1976.
80. Carew TJ, Walters ET, Kandel ER. Associative learning in Aplysia: cellular correlates supporting a conditioned fear hypothesis. Science 1981; 211: 501-504.
81. Cohen DH. Involvement of the avian amygdalar homologue (archistriatum posterior and mediale) in defensively conditioned heart rate change. J Comp Neurol 1975; 160: 13-35.
82. Thompson RF. The neurobiology of learning and memory. Science 1986; 233: 941-947.
83. Kapp BS, Frysinger RC, Gallagher M, Haselton JR. Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 1979; 23: 1109-1117.
84. Davis M. Sensitization of the acoustic startle reflex by footshock. Behav Neurosci 1989; 103: 495-503.
85. Kamin LJ, Brimer CJ, Black AH. Conditioned suppression as a monitor of fear ofthe CS in the course of avoidance training. J Comp Physiol Psychol 1963; 56: 497-501.
86. Blanchard RJ, Blanchard DC. Crouching as an index of fear. J Comp Physiol Psychol 1969; 67: 370-375.
87. Stebbins WC, Smith OA. Cardiovascular concomitants of the conditioned emotional response in monkey. Science 1964; 144: 881-883.
88. Heimer L, Robards MJ. Neuroanatomical Tract-Tracing Methods. Plenum Press: New York, NY, USA, 1981.
89. Emson PC. Chemical Neuroanatomy. Raven Press, 1983.
90. Solomon RL, Kamin LJ, Wynne LC. Traumatic avoidance learning: the outcomes of several extinction procedures with dogs. J Abnorm Psychol 1953; 48: 291-302.
91. Bolles RC, Fanselow MS. A perceptual-defensive-recuperative model of fear and pain. Behav Brain Sci 1980; 3: 291-323.
92. Annau Z, Kamin LJ. The conditioned emotional response as a function of the intensity of the US. J Comp Physiol Psychol 1961; 54: 428-432.
93. Starr MD, Mineka S. Determinants of fear over the course of avoidance learning. Learn Motiv 1977; 8: 331-350.
94. Lang PJ. Fear reduction and fear behavior: problems in treating a construct. In: Schlien JM (ed). Research in Psychotherapy vol. 3. American Psychological Association: Washington, DC, USA, 1968 pp 90-103.
95. Zinbarg RE. Concordance and synchrony in measures of anxiety and panic reconsidered: a hierarchical model of anxiety and panic. Behav Ther 1998; 29: 301-323.
96. Bindra D. A unified interpretation of emotion and motivation. Ann N Y Acad Sci 1969; 159: 1071-1083.
97. Bolles RC. Theory of Motivation. Harper and Row: New York, NY, USA, 1967.
98. Logan FA, Wagner AR. Reward and Punishment. Allyn and Bacon: Boston, MA, USA, 1965.
99. Davis M, Hitchcock JM, Rosen JB. Anxiety and the amygdala: pharmacological and anatomical analysis of the fear-potentiated startle paradigm. In: Bower GH (ed). The Psychology of Learning and Motivation vol 21. Academic Press: San Diego, CA, USA, 1987 pp 263-305.
100. LeDoux JE. The Emotional Brain. Simon and Schuster: New York, NY, USA, 1996.
101. Lang PJ, Bradley MM, Cuthbert BN. Emotion, attention, and the startle reflex. Psychol Rev 1990; 97: 377-395.
102. Lang PJ, Davis M. Emotion, motivation, and the brain: reflex foundations in animal and human research. Prog Brain Res 2006; 156: 3-29.
103. Adolphs R. The biology of fear. Curr Biol 2013; 23: R79-R93.
104. Perusini JN, Fanselow MS. Neurobehavioral perspectives on the distinction between fear and anxiety. Learn Mem 2015; 22: 417-425.
105. Fanselow MS. Neural organization of the defensive behavior system responsible for fear. Psychon Bull Rev 1994; 1: 429-438.
106. Panksepp J. Affective Neuroscience. Oxford University Press: New York, NY, USA, 1998.
107. Panksepp J, Fuchs T, Iacabucci P. The basic neuroscience of emotional experiences in mammals: the case of subcortical FEAR circuitry and implications for clinical anxiety. Appl Anim Behav Sci 2011; 129: 1-17.
108. Rau V, DeCola JP, Fanselow MS. Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 2005; 29: 1207-1223.
109. Milad MR, Quirk GJ. Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 2012; 63: 129-151.
110. Marx MH. Intervening variable or hypothetical construct? Psychol Rev 1951; 58: 235-247.
111. LeDoux J. Rethinking the emotional brain. Neuron 2012; 73: 653-676.
112. LeDoux JE. Coming to terms with fear. Proc Natl Acad Sci USA 2014; 111: 2871-2878.
113. LeDoux JE. The slippery slope of fear. Trends Cogn Sci 2013; 17: 155-156.
114. Dolan RJ, Vuilleumier P. Amygdala automaticity in emotional processing. Ann N Y Acad Sci 2003; 985: 348-355.
115. Mineka S, Ohman A. Phobias and preparedness: the selective, automatic, and encapsulated nature of fear. Biol Psychiatry 2002; 52: 927-937.
116. Vuilleumier P, Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 2007; 45: 174-194.
117. Whalen PJ, Kagan J, Cook RG, Davis FC, Kim H, Polis S et al. Human amygdala responsivity to masked fearful eye whites. Science 2004; 306: 2061.
118. Luo Q, Holroyd T, Majestic C, Cheng X, Schechter J, Blair RJ. Emotional auto-maticity is a matter of timing. J Neurosci 2010; 30: 5825-5829.
119. Lissek S, Levenson J, Biggs AL, Johnson LL, Ameli R, Pine DS et al. Elevated fear conditioning to socially relevant unconditioned stimuli in social anxiety disorder. Am J Psychiatry 2008; 165: 124-132.
120. Hariri AR, Tessitore A, Mattay VS, Fera F, Weinberger DR. The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 2002; 17: 317-323.
121. Anderson AK, Phelps EA. Is the human amygdala critical for the subjective experience of emotion? Evidence of intact dispositional affect in patients with amygdala lesions. J Cogn Neurosci 2002; 14: 709-720.
122. Feinstein JS, Buzza C, Hurlemann R, Follmer RL, Dahdaleh NS, Coryell WH et al. Fear and panic in humans with bilateral amygdala damage. Nat Neurosci 2013; 16: 270-272.
123. Phelps EA. Emotion and cognition: insights from studies of the human amygdala. Annu Rev Psychol 2006; 57: 27-53.
124. Weiskrantz L. Consciousness Lost and Found: A Neuropsychological Exploration. Oxford University Press: New York, NY, USA, 1997.
125. Morris JS, DeGelder B, Weiskrantz L, Dolan RJ. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 2001; 124(Pt 6): 1241-1252.
126. Tamietto M, de Gelder B. Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 2010; 11: 697-709.
127. Bertini C, Cecere R, Ladavas E. I am blind, but I "see" fear. Cortex 2013; 49: 985-993.
128. LeDoux J, Pine DS. Using neuroscience to help understand fear and anxiety: a two-system framework. Am J Psychiatry; advance online publication, 9 September; appiajp201616030353 [e-pub ahead of print].
129. Downey G, Mougios V, Ayduk O, London BE, Shoda Y. Rejection sensitivity and the defensive motivational system: insights from the startle response to rejection cues. Psychol Sci 2004; 15: 668-673.
130. Lang PJ, Bradley MM. Appetitive and defensive motivation: goal-directed or goal-determined? Emot Rev 2013; 5: 230-234.
131. Dickinson A, Balleine B. The role of learning in the operation of motivational systems. In: Gallistel CR (ed). Steven's Handbook of Experimental Psychology: Learning, Motivation and Emotion3rd ednvol. 3. John Wiley & Sons: New York, NY, USA, 2002 pp 497-534.
132. Church RM. Systematic effect of random error in the yoked control design. Psychol Bull 1964; 62: 122-131.
133. Church RM. The yoked control design. In: Archer T, Nilsson L (eds). Aversion, Avoidance and Anxiety: Perspectives on Aversively Motivated Behavior. Erlbaum: Hillsdale, NJ, USA, 1989 pp 403-413.
134. Clarke RJ. Flight behaviour elicited by electrical stimulation of the hypothalamus and midbrain in rats: escape and avoidance properties. Master of Science thesis, University of British Columbia, Vancouver, Canada 1972.
135. Brown JL, Hunsperger RW, Rosvold HE. Defence, attack, and flight elicited by electrical stimulation of the hypothalamus of the cat. Exp Brain Res 1969; 8: 113-129.
136. Cardinal RN, Parkinson JA, Hall J, Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002; 26: 321-352.
137. Dickinson A. Action and habits: the development of behavioural autonomy. Philos Trans R Soc Lond B Biol Sci 1985; 308: 67-78.
138. Dezfouli A, Balleine BW. Habits, action sequences and reinforcement learning. Eur J Neurosci 2012; 35: 1036-1051.
139. Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005; 8: 1481-1489.
140. Balleine BW, O'Doherty JP. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsycho-pharmacology 2010; 35: 48-69.
141. Choi JS, Cain CK, LeDoux JE. The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem 2010; 17: 139-147.
142. Lazaro-Munoz G, LeDoux JE, Cain CK. Sidman instrumental avoidance initially depends on lateral and Basal amygdala and is constrained by central amygdala-mediated Pavlovian processes. Biol Psychiatry 2010; 67: 1120-1127.
143. Mackintosh NJ. The Psychology of Animal Learning. Academic Press: New York, NY, USA, 1974.
144. Dickinson A. Instrumental conditioning. In: Mackintosh NJ (ed). Animal Learning and Cognition. Academic Press: San Diego, CA, USA, 1994 pp 45-79.
145. Rescorla RA. Evidence for an association between the discriminative stimulus and the response-outcome association in instrumental learning. J Exp Psychol Anim Behav Process 1990; 16: 326-334.
146. Balleine B, Dickinson A. Instrumental performance following reinforcer devaluation depends upon incentive learning. Q J Exp Psychol B 1991; 43: 279-296.
147. Holland PC. Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process 2004; 30: 104-117.
148. Holland PC. Cognitive versus stimulus-response theories of learning. Learn Behav 2008; 36: 227-241.
149. Mackintosh NJ. Conditioning and Associative Learning. Oxford University Press: New York, NY, USA, 1983.
150. Dickinson A, Boakes RA (eds). Mechanisms of Learning and Motivation: A Memorial Volume to Jerzy Konorski. Erlbaum: Hillsdale, NJ, USA, 1979.
151. Cain CK, LeDoux JE. Escape from fear: a detailed behavioral analysis of two atypical responses reinforced by CS termination. J Exp Psychol Anim Behav Process 2007; 33: 451-463.
152. Amorapanth P, LeDoux JE, Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 2000; 3: 74-79.
153. Rescorla RA. Pavlovian conditioned fear in Sidman avoidance learning. J Comp Physiol Psychol 1968; 65: 55-60.
154. Morris RGM. Pavlovian conditioned inhibition of fear during shuttlebox avoidance behavior. Learn Motiv 1974; 5: 424-447.
155. De Houwer J, Crombez G, Baeyens F. Avoidance behavior can function as a negative occasion setter. J Exp Psychol Anim Behav Process 2005; 31: 101-106.
156. Moscarello JM, LeDoux JE. Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J Neurosci 2013; 33: 3815-3823.
157. LeDoux JE. Emotion and the amygdala. In: Aggleton JP (ed). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss: New York, NY, USA, 1992 pp 339-351.
158. Davis M. The role of the amygdala in conditioned fear. In: Aggleton JP (ed). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss: New York, NY, USA, 1992 pp 255-306.
159. Kapp BS, Whalen PJ, Supple WF, Pascoe JP. Amygdaloid contributions to conditioned arousal and sensory information processing. In: Aggleton JP (ed). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss: New York, NY, USA, 1992 pp 229-254.
160. Maren S. Synaptic mechanisms of associative memory in the amygdala. Neuron 2005; 47: 783-786.
161. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 1987; 264: 123-146.
162. Romanski LM, LeDoux JE, Clugnet MC, Bordi F. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci 1993; 107: 444-450.
163. Bordi F, LeDoux JE. Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp Brain Res 1994; 98: 275-286.
164. Rogan MT, LeDoux JE. LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 1995; 15: 127-136.
165. Rogan MT, Staubli UV, LeDoux JE. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997; 390: 604-607.
166. Quirk GJ, Armony JL, LeDoux JE. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 1997; 19: 613-624.
167. Quirk GJ, Repa C, LeDoux JE. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 1995; 15: 1029-1039.
168. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 2001; 4: 724-731.
169. Maren S. Auditory fear conditioning increases CS-elicited spike firing in lateral amygdala neurons even after extensive overtraining. Eur J Neurosci 2000; 12: 4047-4054.
170. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM. The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. J Neurosci 1990; 10: 1062-1069.
171. Muller J, Corodimas KP, Fridel Z, LeDoux JE. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 1997; 111: 683-691.
172. Nader K, Majidishad P, Amorapanth P, LeDoux JE. Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 2001; 8: 156-163.
173. Grundemann J, Luthi A. Ensemble coding in amygdala circuits for associative learning. Curr Opin Neurobiol 2015; 35: 200-206.
174. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 2001; 8: 229-242.
175. Rodrigues SM, Schafe GE, LeDoux JE. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004; 44: 75-91.
176. Pitkänen A, Savander V, LeDoux JE. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 1997; 20: 517-523.
177. Pare D, Smith Y. Intrinsic circuitry of the amygdaloid complex: common principles of organization in rats and cats. Trends Neurosci 1998; 21: 240-241.
178. Royer S, Martina M, Pare D. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 1999; 19: 10575-10583.
179. Pascoe JP, Kapp BS. Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 1985; 16: 117-133.
180. Wilensky AE, Schafe GE, Kristensen MP, LeDoux JE. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of pavlovian fear conditioning. J Neurosci 2006; 26: 12387-12396.
181. Duvarci S, Popa D, Pare D. Central amygdala activity during fear conditioning. J Neurosci 2011; 31: 289-294.
182. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010; 468: 277-282.
183. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010; 468: 270-276.
184. Li H, Penzo MA, Taniguchi H, Kopec CD, Huang ZJ, Li B. Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci 2013; 16: 332-339.
185. LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 1988; 8: 2517-2529.
186. Hitchcock JM, Davis M. Fear-potentiated startle using an auditory conditioned stimulus: effect of lesions of the amygdala. Physiol Behav 1987; 39: 403-408.
187. Kim JJ, Rison RA, Fanselow MS. Effects of amygdala, hippocampus, and peria-queductal gray lesions on short-and long-term contextual fear. Behav Neurosci 1993; 107: 1093-1098.
188. LaBar KS, LeDoux JE, Spencer DD, Phelps EA. Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci 1995; 15: 6846-6855.
189. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995; 269: 1115-1118.
190. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 1998; 20: 937-945.
191. Morris JS, Ohman A, Dolan RJ. A subcortical pathway to the right amygdala mediating "unseen" fear. Proc Natl Acad Sci USA 1999; 96: 1680-1685.
192. Morris JS, Ohman A, Dolan RJ. Conscious and unconscious emotional learning in the human amygdala. Nature 1998; 393: 467-470.
193. Mendez-Bertolo C, Moratti S, Toledano R, Lopez-Sosa F, Martinez-Alvarez R, Mah YH et al. A fast pathway for fear in human amygdala. Nat Neurosci 2016; 19: 1041-1049.
194. Cain CK, Choi JS, LeDoux JE. Active avoidance and escape learning. In: Koob G, Thompson R, Le Moal M (eds). Encyclopedia of Behavioral Neuroscience. Elsevier: New York, NY, USA, 2010.
195. Moscarello JM, LeDoux J. Diverse effects of conditioned threat stimuli on behavior. Cold Spring Harb Symp Quant Biol 2014; 79: 11-19.
196. Maren S, Poremba A, Gabriel M. Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain Res 1991; 549: 311-316.
197. Poremba A, Gabriel M. Medial geniculate lesions block amygdalar and cingulothalamic learning-related neuronal activity. J Neurosci 1997; 17: 8645.
198. Gabriel M, Burhans L, Kashef A. Consideration of a unified model of amygdalar associative functions. Ann N Y Acad Sci 2003; 985: 206-217.
199. McDonald AJ. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neurosci 1991; 44: 15-33.
200. Groenewegen HJ, Wright CI, Beijer AV, Voorn P. Convergence and segregation of ventral striatal inputs and outputs. Ann N Y Acad Sci 1999; 877: 49-63.
201. Wright CI, Beijer AV, Groenewegen HJ. Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 1996; 16: 1877-1893.
202. Blackburn JR, Pfaus JG, Phillips AG. Dopamine functions in appetitive and defensive behaviours. Prog Neurobiol 1992; 39: 247-279.
203. Carelli RM. Nucleus accumbens cell firing and rapid dopamine signaling during goal-directed behaviors in rats. Neuropharmacology 2004; 47(Suppl 1): 180-189.
204. Kelley AE. Functional specificity of ventral striatal compartments in appetitive behaviors. Ann N Y Acad Sci 1999; 877: 71-90.
205. Everitt BJ, Parkinson JA, Olmstead MC, Arroyo M, Robledo P, Robbins TW. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann N Y Acad Sci 1999; 877: 412-438.
206. Berridge KC. 'Liking' and 'wanting' food rewards: brain substrates and roles in eating disorders. Physiol Behav 2009; 97: 537-550.
207. Burhans LB, Gabriel M. Contextual modulation of conditioned responses: role of the ventral subiculum and nucleus accumbens. Behav Neurosci 2007; 121: 1243-1257.
208. Shiflett MW, Balleine BW. At the limbic-motor interface: disconnection of baso-lateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation. Eur J Neurosci 2010; 32: 1735-1743.
209. Robbins TW, Cador M, Taylor JR, Everitt BJ. Limbic-striatal interactions in reward-related processes. Neurosci Biobehav Rev 1989; 13: 155-162.
210. Cador M, Robbins TW, Everitt BJ. Involvement of the amydala in stimulus-reward associations: interaction with the ventral striatum. Neurosci 1989; 30: 77-86.
211. Ramirez F, Moscarello JM, LeDoux JE, Sears RM. Active avoidance requires a serial Basal amygdala to nucleus accumbens shell circuit. J Neurosci 2015; 35: 3470-3477.
212. Wenzel JM, Rauscher NA, Cheer JF, Oleson EB. A role for phasic dopamine release within the nucleus accumbens in encoding aversion: a review of the neurochemical literature. ACS Chem Neurosci 2015; 6: 16-26.
213. Nakanishi S, Hikida T, Yawata S. Distinct dopaminergic control of the direct and indirect pathways in reward-based and avoidance learning behaviors. Neu-roscience 2014; 282C: 49-59.
214. Lichtenberg NT, Kashtelyan V, Burton AC, Bissonette GB, Roesch MR. Nucleus accumbens core lesions enhance two-way active avoidance. Neuroscience 2014; 258: 340-346.
215. Oleson EB, Cheer JF. On the role of subsecond dopamine release in conditioned avoidance. Front Neurosci 2013; 7: 96.
216. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM. Dopamine operates as a subsecond modulator of food seeking. J Neurosci 2004; 24: 1265-1271.
217. Martinez RC, Gupta N, Lazaro-Munoz G, Sears RM, Kim S, Moscarello JM et al. Active vs. reactive threat responding is associated with differential c-Fos expression in specific regions of amygdala and prefrontal cortex. Learn Mem 2013; 20: 446-452.
218. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 2005; 8: 365-371.
219. Poremba A, Gabriel M. Amygdala neurons mediate acquisition but not maintenance of instrumental avoidance behavior in rabbits. J Neurosci 1999; 19: 9635-9641.
220. Everitt BJ, Robbins TW. Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol 2016; 67: 23-50.
221. Delgado MR, Jou RL, LeDoux JE, Phelps EA. Avoiding negative outcomes: tracking the mechanisms of avoidance learning in humans during fear conditioning. Front Behav Neurosci 2009; 3: 33.
222. Collins KA, Mendelsohn A, Cain CK, Schiller D. Taking action in the face of threat: neural synchronization predicts adaptive coping. J Neurosci 2014; 34: 14733-14738.
223. Schlund MW, Hudgins CD, Magee S, Dymond S. Neuroimaging the temporal dynamics of human avoidance to sustained threat. Behav Brain Res 2013; 257: 148-155.
224. Rachman S. The passing of the two-stage theory of fear and avoidance: fresh possibilities. Behav Res Ther 1976; 14: 125-131.
225. Bouton ME, Mineka S, Barlow DH. A modern learning theory perspective on the etiology of panic disorder. Psychol Rev 2001; 108: 4-32.
226. LeDoux JE, Gorman JM. A call to action: overcoming anxiety through active coping. Am J Psychiatry 2001; 158: 1953-1955.
227. van der Kolk B. The Body Keeps the Score: Brain, Mind, and Body in the Healing of Trauma. Viking: New York, NY, USA, 2014.
228. Raio CM, Phelps EA. The influence of acute stress on the regulation of conditioned fear. Neurobiol Stress 2015; 1: 134-146.
229. Maier SF, Watkins LR. Role of the medial prefrontal cortex in coping and resilience. Brain Res 2010; 1355: 52-60.
230. Gillan CM, Morein-Zamir S, Urcelay GP, Sule A, Voon V, Apergis-Schoute AM et al. Enhanced avoidance habits in obsessive-compulsive disorder. Biol Psychiatry 2014; 75: 631-638.
231. Cuthbert BN, Insel TR. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med 2013; 11: 126.
232. Poulton R, Menzies RG. Fears born and bred: toward a more inclusive theory of fear acquisition. Behav Res Ther 2002; 40: 197-208.
233. McNally RJ. On nonassociative fear emergence. Behav Res Ther 2002; 40: 169-172.