Sidman Instrumental Avoidance Initially Depends on Lateral and Basal Amygdala and Is Constrained by Central Amygdala-Mediated Pavlovian Processes

Biological Psychiatry

Volumn 67, Issue 12, 2010, Pages 1120-1127

  Lázaro Muñoz, Gabriel ^a   LeDoux, Joseph E ^a,b   Cain, Christopher K ^a  

^a NEW YORK UNIVERSITY   (United States)

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

Author keywords

Amygdala; avoidance; freezing; lesion; Sidman

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; CONDITIONING; CONTROLLED STUDY; DEFENSE MECHANISM; FREEZING; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; TRAINING; ANATOMY AND HISTOLOGY; ANIMAL; CONDITIONED REFLEX; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMYGDALA; ANIMALS; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77952888164     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.12.002     Document Type: Article

References (82)

1. Bolles R.C., and Collier A.C. The effect of predictive cues on freezing in rats. Anim Learn Behav 4 (1976) 6-8
2. Hirsh S.M., and Bolles R.C. On the ability of prey to recognize predators. Z Fur Tierpsychol 54 (1980) 71-84
3. Fanselow M.S., and Lester L.S. A functional behavioristic approach to aversively motivated behavior: Imminence as a determinant of the topography of defensive behavior. In: Bolles R.C., and Bleecher M.D. (Eds). Evolution and Learning (1988), Erlbaum, Hillsdale, NJ 185-211
4. Bolles R.C. Species-specific defense reactions and avoidance learning. Psychol Rev 77 (1970) 32-48
5. Blanchard R.J., Flannelly K.J., and Blanchard D.C. Defensive behaviors of laboratory and wild Rattus norvegicus. J Comp Psychol 100 (1986) 101-107
6. Solomon R.L., and Wynne L.C. Traumatic avoidance learning: The principles of anxiety conservation and partial irreversibility. Psychol Rev 61 (1954) 353-385
7. Cain C.K., and LeDoux J.E. Escape from fear: A detailed behavioral analysis of two atypical responses reinforced by CS termination. J Exp Psych: Anim Behav Process 33 (2007) 451-463
8. Rodrigues S.M., Ledoux J.E., and Sapolsky R.M. The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32 (2009) 289-313
9. Roozendaal B., McEwen B.S., and Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 10 (2009) 423-433
10. Sapolsky R.M. The influence of social hierarchy on primate health. Science 308 (2005) 648-652
11. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. (2000), American Psychiatric Association, Washington, DC
12. NIMH. Anxiety disorders (2007), National Institute of Mental Health, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD
13. LeDoux J.E., and Gorman J.M. A call to action: Overcoming anxiety through active coping. Am J Psychiatry 158 (2001) 1953-1955
14. van der Kolk B.A. Clinical implications of neuroscience research in PTSD. Ann N Y Acad Sci 1071 (2006) 277-293
15. Cain C.K., and LeDoux J.E. Brain mechanisms of Pavlovian and instrumental aversive conditioning. In: Nutt D.J., Blanchard R.J., Blanchard D.C., and Griebel G. (Eds). Handbook of Anxiety and Fear Vol 17 (2008), Elsevier Academic, Amsterdam 103-125
16. Keay K.A., and Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 25 (2001) 669-678
17. Blanchard R.J., and Blanchard D.C. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 81 (1972) 281-290
18. Davis M. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: Aggleton J.P. (Ed). The Amygdala (2000), Oxford University Press, Oxford, UK 213-288
19. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 23 (2000) 155-184
20. Fanselow M.S., and Gale G.D. The amygdala, fear, and memory. Ann N Y Acad Sci 985 (2003) 125-134
21. Paré D., Royer S., Smith Y., and Lang E.J. Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann N Y Acad Sci 985 (2003) 78-91
22. LeDoux J.E. The amygdala. Curr Biol 17 (2007) 868-879
23. Fanselow M.S., and LeDoux J.E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23 (1999) 229-232
24. Nader K., Majidishad P., Amorapanth P., and LeDoux J.E. Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 8 (2001) 156-163
25. Gale G.D., Anagnostaras S.G., Godsil B.P., Mitchell S., Nozawa T., Sage J.R., et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. Neuroscience 24 (2004) 3810-3815
26. Wilensky A.E., Schafe G.E., Kristensen M.P., and LeDoux J.E. Rethinking the fear circuit: The central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 26 (2006) 12387-12396
27. Maren S. Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J Neurosci 19 (1999) 8696-8703
28. LeDoux J.E., Cicchetti P., Xagoraris A., and Romanski L.M. The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. J Neurosci 10 (1990) 1062-1069
29. Campeau S., and Davis M. Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15 (1995) 2301-2311
30. Paré D., Quirk G.J., and LeDoux J.E. New vistas on amygdala networks in conditioned fear. J Neurophysiol 92 (2004) 1-9
31. Amorapanth P., LeDoux J.E., and Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 3 (2000) 74-79
32. Anglada-Figueroa D., and Quirk G.J. Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25 (2005) 9680-9685
33. Herry C., Ciocchi S., Senn V., Demmou L., Muller C., and Lüthi A. Switching on and off fear by distinct neuronal circuits. Nature 454 (2008) 600-606
34. Goddard G.V. Functions of the amygdala. Psychol Rev 62 (1964) 89-109
35. Sarter M.F., and Markowitsch H.J. Involvement of the amygdala in learning and memory: A critical review, with emphasis on anatomical relations. Behav Neurosci 99 (1985) 342-380
36. Maren S., Poremba A., and Gabriel M. Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain Res 549 (1991) 311-316
37. Killcross S., Robbins T.W., and Everitt B.J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388 (1997) 377-380
38. Poremba A., and Gabriel M. Amygdalar lesions block discriminative avoidance learning and cingulothalamic training-induced neuronal plasticity in rabbits. J Neurosci 17 (1997) 5237-5244
39. Poremba A., and Gabriel M. Amygdala neurons mediate acquisition but not maintenance of instrumental avoidance behavior in rabbits. J Neurosci 19 (1999) 9635-9641
40. Holahan M.R., and White N.M. Amygdala inactivation blocks expression of conditioned memory modulation and the promotion of avoidance and freezing. Behav Neurosci 118 (2004) 24-35
41. Rorick-Kehn L.M., and Steinmetz J.E. Amygdalar unit activity during three learning tasks: Eyeblink classical conditioning, Pavlovian fear conditioning, and signaled avoidance conditioning. Behav Neurosci 119 (2005) 1254-1273
42. Brush F.R. On the difference between animals that learn and do not learn to avoid electric shock. Psychon Sci 5 (1966) 123-124
43. Brush F.R. Selection for differences in avoidance learning: The Syracuse strains differ in anxiety, not learning ability. Behav Genet 33 (2003) 677-696
44. Bolles R.C., and Popp Jr. R.J. Parameters affecting the acquisition of Sidman avoidance. J Exp Anal Behav 7 (1964) 315-321
45. Choi J., and LeDoux J.E. Lesions of the lateral/basal but not the central nucleus of the amygdala impair post-training performance of fear-induced 2-way active avoidance signaled by a conditioned stimulus: Program Number 623.5. Abstract Viewer/Itinerary Planner (2003), Society for Neuroscience, Washington, DC. http://www.sfn.org/index.cfm?pagename=abstracts_archive&task=view&controlID=10799&year=2003 Accessed January 7, 2010
46. Schwartzbaum J.S., Green R.H., Beatty W.W., and Thompson J.B. Acquisition of avoidance behavior following septal lesions in the rats. J Comp Physiol Psychol 63 (1967) 95-104
47. Blanchard R.J., and Blanchard D.C. Reactive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 68 (1969) 129-135
48. Blanchard R.J., Blanchard D.C., and Fial R.A. Hippocampal lesions in rats and their effect on activity, avoidance, and aggression. J Comp Physiol Psychol 71 (1970) 92-102
49. Anisman H., and Waller T.G. Facilitative and disruptive effects of prior exposure to shock on subsequent avoidance performance. J Comp Physiol Psychol 78 (1972) 113-122
50. Overmier J.B., and Seligman M.E. Effects of inescapable shock upon subsequent escape and avoidance responding. J Comp Physiol Psychol 63 (1967) 28-33
51. Overmier J.B. Interference with avoidance behavior: Failure to escape traumatic shock. J Exp Psychol 78 (1968) 340-343
52. Bignami G. Selection for high rates and low rates of avoidance conditioning in the rat. Anim Behav 13 (1965) 221-227
53. Brush F.R., Froehlich J.C., and Sakellaris P.C. Genetic selection for avoidance behavior in the rat. Behav Genet 9 (1979) 309-316
54. Ryzhova L.I., Kulagin D.A., and Lopatina N.G. Correlated variability in motor activity and emotionality in selecting rats for high and low values of active avoidance conditioned reflexes. Genetika 19 (1983) 121-125
55. Blizard D.A., and Adams N. The Maudsley reactive and nonreactive strains: A new perspective. Behav Genet 32 (2002) 277-299
56. Servatius R.J., Jiao X., Beck K.D., Pang K.C., and Minor T.R. Rapid avoidance acquisition in Wistar-Kyoto rats. Behav Brain Res 192 (2008) 191-197
57. Sidman M. Avoidance conditioning with brief shock and no exteroceptive warning signal. Science 118 (1953) 157-158
58. Sidman M. Two temporal parameters of the maintenance of avoidance behavior by the white rat. J Comput Physiol Pshycol 46 (1953) 253-261
59. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 5th ed. (2005), Elsevier/Academic Press, San Diego
60. Blanchard R.J., and Blanchard D.C. Crouching as an index of fear. J Comp Physiol Psychol 67 (1969) 370-375
61. King F.A. Effects of septal and amygdaloid lesions on emotional behavior and conditioned avoidance responses in the rat. J Nerv Ment Dis 126 (1958) 57-63
62. Grossman S.P., Grossman L., and Walsh L. Functional organization of the rat amygdala with respect to avoidance behavior. J Comp Physiol Psychol 88 (1975) 829-850
63. Roozendaal B., Koolhaas J.M., and Bohus B. The central amygala is involved in conditioning but not retention of active and reactive shock avoidance in male rats. Behav Neural Biol 59 (1993) 143-149
64. Isaacson R.L., Douglas R.J., and Moore R.Y. The effect of radical hippocampal ablation on acquisition of avoidance response. J Comp Physiol Psychol 54 (1961) 625-628
65. Cain C.K., and LeDoux J.E. Emotional processing and motivation: In search of brain mechanisms. In: Elliot A.J. (Ed). Handbook of Approach and Avoidance Motivation (2008), Psychology Press, Taylor and Francis Group, New York 17-34
66. Balleine B.W., and Killcross S. Parallel incentive processing: An integrated view of amygdala function. Trends Neurosci 39 (2006) 272-279
67. Zimmerman J.M., Rabinak C.A., McLachlan I.G., and Maren S. The central nucleus of the amygdala is essential for acquiring and expressing conditional fear after overtraining. Learn Mem 14 (2007) 634-644
68. Poulus A.M., Li V., Sterlace S.S., Tokushige F., Ponnusamy R., and Fanselow M.S. Persistence of fear memory across time requires the basolateral amygdala complex. Proc Natl Acad Sci USA 106 (2009) 11737-11741
69. Krieckhaus E.E., Simmons H.J., Thomas G.J., and Kenyon J. Septal lesions enhance shock avoidance behavior in the rat. Exp Neurol 9 (1964) 107-113
70. de Oca B.M., Minor T.R., and Fanselow M.S. Brief flight to a familiar enclosure in response to a conditional stimulus in rats. J Gen Psychol 134 (2007) 153-172
71. Davis M., and Shi C. The extended amygdala: Are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety?. Ann N Y Acad Sci 877 (1999) 281-291
72. Pitkänen A. Connectivity of the rat amygdaloid complex. In: Aggleton J.P. (Ed). The Amygdala (2000), Oxford University Press, Oxford, UK 31-116
73. Sullivan G.M., Apergis J., Bush D.E., Johnson L.R., Hou M., and LeDoux J.E. Lesions of the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128 (2004) 7-14
74. LeDoux J.E., Iwata J., Cicchetti P., and Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8 (1988) 2517-2529
75. Kim J.J., Rison R.A., and Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 107 (1993) 1093-1098
76. Amorapanth P., Nader K., and LeDoux J.E. Lesions of periaqueductal gray dissociate-conditioned freezing from conditioned suppression behavior in rats. Learn Mem 6 (1999) 491-499
77. Jallestad F.K., Markowska A., and Bakke H.K. Behavioral effects after ibotenic acid, 6- OHDA and electrolytic lesions in the central amygdala nucleus of the rat. Physiol Behav 37 (1986) 855-862
78. Werka T., and Zielinski K. CS modality transfer of two-way avoidance in rats with central and basolateral amygdala lesions. Behav Brain Res 93 (1998) 11-24
79. Kessler R.C., Heeringa S., Lakoma M.D., Petukhova M., Rupp A.E., Schoenbaum M., et al. The individual-level and societal-level effects of mental disorders on earnings in the United States: Results from the national comorbidity survey replication. Am J Psychiatry 165 (2008) 703-711
80. Cloitre M. Effective psychotherapies for posttraumatic stress disorder: A review and critique. CNS Spectr 14 (2009) 32-43
81. Kamin L.J., Brimer C.J., and Black A.H. Conditioned suppression as a monitor of fear of the CS during the course of avoidance training. J Comp Physiological Psychology 56 (1962) 497-501
82. Stovall-McClough K.C., and Cloitre M. Unresolved attachment, PTSD, and dissociation in women with childhood abuse histories. J Consult Clin Psychol 74 (2006) 219-228