Advertisement

Neural Systems Involved in Fear Inhibition: Extinction and Conditioned Inhibition

  • Michael Davis
  • William A. Falls
  • Jonathan Gewirtz
Part of the Neurobiological Foundation of Aberrant Behaviors book series (NFAB, volume 1)

Abstract

“I can’t get the memories out of my mind! The images come flooding back in vivid detail, triggered by the most inconsequential things, like a door slamming or the smell of stir-fried pork. Last night, I went to bed, was having a good sleep for a change. Then in the early morning a storm-front passed through and there was a bolt of crackling thunder. I awoke instantly, frozen in fear. I am right back in Viet Nam, in the middle of the monsoon season at my guard post. I am sure I’ll get hit in the next volley and convinced I will die. My hands are freezing, yet sweat pours from my entire body. I feel each hair on the back of my neck standing on end. I can’t catch my breath and my heart is pounding. I smell a damp sulfur smell. Suddenly I see what’s left of my buddy Troy, his head on a bamboo platter, sent back to our camp by the Viet Cong. Propaganda messages are stuffed between his clenched teeth. The next bolt of lightning and clap of thunder makes me jump so much that I fall to the floor..... ” (Paraphrased from a war veteran’s conversations with Dr. R. L. Gelman, Dept. of Psychiatry, Yale University School of Medicine).

Keywords

Conditioned Stimulus Conditioned Fear Inferior Colliculus Medial Prefrontal Cortex Conditioned Inhibition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aggleton, J.P. (1992) The amygdala. Neurochemical aspects of emotion, memory, and mental dysfunction. New York: John Wiley-Liss and Sons.Google Scholar
  2. Annau, Z. and Kamin, L.J. (1961) The conditioned emotional response as a function of US intensity. Journal of Comparative and Physiological Psychology 54: 428–432.PubMedCrossRefGoogle Scholar
  3. Baker, J.D. and Azorlosa, J.L. (1996) The NMDA antagonist MK-801 blocks the extinction of Pavlovian fear conditioning. Behav Neurosci 110: 618–620.PubMedCrossRefGoogle Scholar
  4. Bandler, R. and Shipley, M.T. (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? TINS 17: 379–389.PubMedGoogle Scholar
  5. Berger, T.W., Weiker,t C.L., Basset, J.L., On, W.B. (1986) Lesions of the retrosplinal cortex produce deficits in reversal learning of the rabbit nictitating membrane response: implications for potential interactions between hippocampal and cerebellar brain systems. Behav Neurosci 100: 802–809.Google Scholar
  6. Bolles, R.C. and Fanselow, M.S. (1980) A perceptual-defensive-recuperative model of fear and pain. The behavioral and brain sciences 3: 281–323.Google Scholar
  7. Borowski, T.B. and Kokkinides, L. (1998) The effects of cocaine, amphetamine, and the dopamine D1 receptor agonist SKF 38393 on fear extinction as measured with potentiated startle: Implications for psychomotor stimulant psychosis. Behav Neurosci 112: 952–965.Google Scholar
  8. Bouton, M.D. and Bolles, R.C. (1979a) Role of contextual stimuli in reinstatement of extinguished fear. J Exp Psychol: Animal Behav Process 5: 368–378.Google Scholar
  9. Bouton, M.E. (1993) Context, time and memory retrieval in the interference paradigms of Pavlovian conditioning. Psychological Bulletin 114: 80–99.PubMedCrossRefGoogle Scholar
  10. Bouton, M.E. and Bolles, R.C. (1979b) Contextual control of the extinction of conditioned fear. Learn and Motiv 10: 455–466.Google Scholar
  11. Bouton, M.E. and Bolles, R.C. (1985) Context, event-memories, and extinction. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
  12. Bouton, M.E. and Brooks, D.C. (1993) Time and context effects on performance in a Pavlovian discrimination reversal. Behav Neurosci 19: 165–179.Google Scholar
  13. Bouton, M.E., Kenney, F.A., Rosengard, C. (1990) State-dependent fear extinction with two benzodiazepine tranquilizers. Behav Neurosci 104: 44–55.PubMedCrossRefGoogle Scholar
  14. Bouton, M.E. and King, D.A. (1983) Contextual control of conditioned fear: tests for the associative value of the context. J Exp Psychol: Animal Behav Process 9: 248–256.Google Scholar
  15. Bouton, M.E. and King, D.A. (1986) Effect of context with mixed histories of reinforcement and nonreinforcement. J Exp Psychol: Animal Behav Process 12: 4–15.Google Scholar
  16. Bouton, M.E. and Nelson, J.B. (1994) Context specificity of target versus feature inhibition in a featurenegative discrimination. J Exp Psychol: Animal Behav Process 20: 51–65.Google Scholar
  17. Bouton, M.E. and Swartzentruber, D. (1991) Sources of relapse after extinction in Pavlovian instrumental learning. Clinical Psychological Review 11: 123–140.CrossRefGoogle Scholar
  18. Buchanan, S.L. and Powell, D.A. (1980) Divergencies in Pavlovian conditioned heart rate and eyeblink responses produced by hippocampectomy in the rabbit ( Oryctolagus cuniculus ). Behav Neural Biol 30: 20–38.Google Scholar
  19. Burns, L.H., Everitt, B.J., Kelly, A.E., Robbins, T.W. (1994) Glutamate-dopamine interactions in the ventral striatum: role in locomotor activity and responding with conditioned reinforcement. Psychopharmacology 115: 516–528.PubMedCrossRefGoogle Scholar
  20. Campeau, S. and Davis, M. (1992b) Involvement of the lateral amygdala and perirhinal cortex in fear potentiated startle to acoustic and visual conditioned stimuli. Soc Neurosci Abst 18: 1562.Google Scholar
  21. Campeau, S. and Davis, M. (1995) Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15: 2312–2327.PubMedGoogle Scholar
  22. Campeau, S,. Falls, W.A., Cullinan, W.E., Helmreich, D.L., Davis, M,. and Watson, S.J. (1997) Elicitation and reduction of fear: behavioral and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 78: 1087–1104.CrossRefGoogle Scholar
  23. Campeau, S., Miserendino, M.J.D., Davis, M. (1992) Intra-amygdala infusion of the N-methyl-DAspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus. Behav Neurosci 106: 569–574.PubMedCrossRefGoogle Scholar
  24. Coco, M.L., Kuhn, C.M., Ely, T.D., Kilts, C.D. (1992) Selective activation of mesoamygdaloïd dopamine neurons by conditioned stress: attenuation by diazepam. Brain Res 590: 39–47.PubMedCrossRefGoogle Scholar
  25. Cox, J. and Westbrook, R.F. (1994) The NMDA receptor antagonist MK-801 blocks acquisition and extinction of conditioned hypoalgesia responses in the rat. Quarterly Journal of Experimental Psychology 47B: 187–210.PubMedGoogle Scholar
  26. Davis, M,. Rainnie, D., Cassell, M. (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends in Neuroscience 17: 208–214.CrossRefGoogle Scholar
  27. DeOca, B.M., DeCola, J.P., Maren, S., Fanselow, M.S. (1998) Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses. The Journal of Neuroscience: 3426–3432.Google Scholar
  28. Deutch, A.Y., Clark, W.A., Roth, R.H. (1990) Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress. Brain Res 521: 311–315.PubMedCrossRefGoogle Scholar
  29. Dickinson, A. and Pearce, J.M. (1977) Inhibitory interactions between appetitive and aversive stimuli. Psychologcal Bulletin 84: 690–711.CrossRefGoogle Scholar
  30. Douglas, R.J. (1972) Inhibition and learning. Pavlovian conditioning in the brain. London: Academic Press.Google Scholar
  31. Estes, W. (1955) Statistical theory of spontaneous recovery and regression. Psychology Review 62: 145154.Google Scholar
  32. Falls, W.A., Bakken, S., and Heldt, S.A. (1997) Lesions of the perirhinal cortex block conditioned excitation but not conditioned inhibition of fear. Behav Neurosci 111: 476–486.PubMedCrossRefGoogle Scholar
  33. Falls, A. and Davis, M. (1995a) Behavioral and physiological analysis of fear inhibition. In: M. J. Friedman, Charney D. S. and Deutch A. Y., eds. Neurobiological and clinical consequences of stress: From normal adaptation to PTSD. Philadelphia: Lippincott-Raven Publishers.Google Scholar
  34. Falls, W.A. and Davis, M, (1995b) Lesions of the central nucleus of the amygdala block conditioned excitation, but not conditioned inhibition of fear as measured with the fear-potentiated startle effect. Behav Neurosci 109: 379–387.PubMedCrossRefGoogle Scholar
  35. Falls, W.A. and Davis, M.J. (1997) Inhibition of fear-potentiated startle can be detected after the offset of a feature trained in a serial feature negative discrimination. Journal of Experimental Psychology: Animal Behavioral Processes 23: 3–14.Google Scholar
  36. Falls, W.A., Josselyn, S.A., Gewirtz, J.C., Pistell, P., and Davis, M. (1998) The nucleus accumbens if not critical for condtioned inhibition of fear as measured with fear-potentiated startle. Soc Neurosci Abst 28:Google Scholar
  37. Falls, W.A., Miserendino, M.J.D., and Davis, M. (1992) Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci 12: 854–863.PubMedGoogle Scholar
  38. Falls, W.F. and Davis, M. (1994) Visual cortex ablations do not prevent extinction of fear-potentiated startle using a visual conditioned stimulus. Behav Neural Bio160: 259–270.Google Scholar
  39. Fanselow, M.S. (1986a) Associative vs. topographical accounts of the immediate shock freezing deficit in rats: Implications for the response selection rules governing species-specific defensive reactions. Learn and Motiv 17: 16–39.Google Scholar
  40. Fanselow, M.S. (1986b) Conditioned fear-induced analgesia: A competing motivational state theory of stress-analgesia. Annuals of the New York Academy of Science 467: 40–54.Google Scholar
  41. Fanselow, M.S. (1991) The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In: A. Depaulis and Bandler R., eds. The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization. New York: Plenum Publishing Co.Google Scholar
  42. Fendt, M. (1998) Different regions of the periaqueductal grey are involved differently in the expression and conditioned inhibition of fear-potentiated startle. European Journal of Neuroscience 10: 387684.Google Scholar
  43. Fendt, M., Koch, M., Schnitzler, H.-U. (1996) Lesions of the central gray block conditioned fear as measured with the potentiated startle paradigm. Behavioural Brain Research 74: 127–134.PubMedCrossRefGoogle Scholar
  44. Fox, G.D. and Holland, P.C. (1998) Neurotoxic hippocampal lesions fail to impair reinstatement of an appetitively conditioned response. Behav Neurosci 112: 255–260.PubMedCrossRefGoogle Scholar
  45. Frohardt, R., Guarraci, F.A., Bouton, M.E. (1999) The effects of neurotoxic hippocampal lesions on two effects of context following fear extinction. Behav Neurosci In press:.Google Scholar
  46. Gewirtz, J. and Davis, M. (1997) Second order fear conditioning prevented by blocking NMDA receptors in the amygdala. Nature 388: 471–474.PubMedCrossRefGoogle Scholar
  47. Gewirtz, J.C., Falls, W.A., Davis, M. (1997) Normal conditioned inhibition and extinction of freezing and fear potentiated startle following electrolytic lesions of medial prefrontal cortex. Behav Neurosci 111: 712–726.PubMedCrossRefGoogle Scholar
  48. Good, M., deHoz, L., Morris, R.G.M. (1998) Contingent versus incidental context processing during conditioning: Dissociation after excitotoxic hippocampal plus dentate gyrus lesions. Hippocampus 8: 147–159.Google Scholar
  49. Graeff, F.G., Silveira, M.C.L., Nogueira, R.L., Audi, E.A., Oliveira, R.M.W. (1993) Role of the amygdala and periaqueductal gray in anxiety and panic. Behav Brain Res 58: 123–131.PubMedCrossRefGoogle Scholar
  50. Guarraci, F.A. and Frohardt, R.J. (1999) Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827: 28–40.PubMedCrossRefGoogle Scholar
  51. Harris, J.A. and Westbrook, R.F. (1998a) Benzodiazepine-induced amnesia in rats: reinstatement of conditioned performance by noxious stimulation on test. Behav Neurosci 112: 183–192.PubMedCrossRefGoogle Scholar
  52. Harris, J.A. and Westbrook, R.F. (1998b) Evidence that GABA transmission mediates context-specific extinction of learned fear. Psychopharmacology 140: 105–115.PubMedCrossRefGoogle Scholar
  53. Harris, J.A. and Westbrook, R.F. (1999) The benzodiazepine midazolam does not impair Pavlovian fear conditioning but regulates when and where fear is expressed. Journal of experimental psychology: Animal behavioral processes 25: 236–246.Google Scholar
  54. Hearst, E. (1972) Some persistent problems in the analysis of conditioned inhibition. In: R. A. Boakes and Halliday M. S., eds. Inhibition and Learning. New York: Academic Press.Google Scholar
  55. Heldt, S.A. and Falls, W.A. (1998) Destruction of the auditory thalamus disrupts the production of fear but not the inhibition of fear conditioned to an auditory stimulus. Brain Res 813: 274–282.PubMedCrossRefGoogle Scholar
  56. Helmstetter, F.J. (1992) The amygdala is essential for the expression of conditioned hypoalgesia. Behav Neurosci 106: 518–528.PubMedCrossRefGoogle Scholar
  57. Helmstetter, F.J. and Tershner,S.A. (1994) Lesions of the periaqueductal gray and rostral ventromedial medulla disrupt antinociceptive but not cardiovascular aversive conditional responses. The Journal of Neuroscience 14: 7099–7108.PubMedGoogle Scholar
  58. Holland, P.C. (1985) The nature of conditioned inhibition in serial and simultaneous feature negative discriminations. In: R. R. Miller and Spear N. E., eds. Information Processing in Animals: Conditioned Inhibition. Hillsdale, N.J.: Lawrence Erlbaum Associates.Google Scholar
  59. Holland, P.C., Lamoureux, J.A., Han, J.-S., Gallagher, M. (1999) Hippocampal lesions interfere with Pavlovian negative ossasion setting. Hippocampus 9: 143–157.PubMedCrossRefGoogle Scholar
  60. Holt, W. and Maren, S. (1999) Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci 19: 9054–9062.PubMedGoogle Scholar
  61. Honey, R.C. and Good, M. (1993) Selective hippocampal lesions abolish the context specificity of latent inhibition and conditioning. Behav Neurosci 107: 23–33.PubMedCrossRefGoogle Scholar
  62. Kehoe, E.J., Macrae, M., Hutchinson, C.L. (1996) MK-801 protects conditioned response from extinction in the rabbit nictitating membrane preparation. Psychobiology 24: 127–135.Google Scholar
  63. Kim, M. and Davis, M. (1993) Electrolytic lesions of the amygdala block acquisition and expression of fear-potentiated startle even with extensive training, but do not prevent re-acquisition. Behav Neurosci 107: 580–595.PubMedCrossRefGoogle Scholar
  64. King, D., Zigmond, M.J., and Finlay, J.M. (1997) Effects of dopamine depletion in the medial prefrontal cortex on the stress-induced increase in extracellular dopamine in the nucleus accumbens core and shell. Neuroscience 77: 141–153.PubMedCrossRefGoogle Scholar
  65. Konorski, J. (1948) Conditioned reflexes and neuronal organization. London: Cambridge University Press.Google Scholar
  66. Konorski, J. (1967) Integrative activity of the brain: An interdisciplinary approach. Chicago: The University of Chicago Press.Google Scholar
  67. Leaton, R.N. and Borszcz, G.S. (1990) Hippocampal lesions and temporally chained conditioned stimuli in a conditioned suppression paradigm. Psychobiology 18: 81–88.Google Scholar
  68. LeDoux, J.E., Romanski, L., Xagoraris, A. (1989) Indelibility of subcortical memories. J Cogn Neurosci 1: 238–243.CrossRefGoogle Scholar
  69. LeDoux, J.E., Sakaguchi, A., Iwata, J., Reis, D.J. (1986a) Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. Neuroscience 17: 615–627.PubMedCrossRefGoogle Scholar
  70. LeDoux, J.E., Sakaguchi, A., Reis, D.J. (1986) Interuption of projections from the medial geniculate mediate emotional responses conditioned to acoustic stimuli. J Neurosci 17: 615–627.CrossRefGoogle Scholar
  71. Lee, H. and Kim, J. (1998) Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. Journal otNeuroscience 18: 8444–8454.Google Scholar
  72. Linke, R., De Lima, A.D., Schwegler, H., Pape, H.C. (1999) Direct synaptic connections of axons from superior colliculus with identified thalamo-amygadloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala. The Journal of Comparative Neurology 403: 158–170.Google Scholar
  73. Lovibond, P.F., Preston, G.C., and Mackintosh, N.J. (1984) Context specificity of conditioning, extinction and latent inhibition. Journal of Experimental Psychology: Animal Behavioral Processes 10: 360–375.Google Scholar
  74. Lubow, R.E. (1989) Latent inhibition and conditioned attention theory. New York: Cambridge University Press.CrossRefGoogle Scholar
  75. Mackintosh, N.J. (1974) The psychology of animal learning. New York: Academic Press.Google Scholar
  76. McAllister, W.R. and McAllister, D.E. (1971) Behavioral measurement of conditioned fear. In: F. R. Brush, ed Aversive Conditioning and Learning. New York: Academic Press.Google Scholar
  77. McGaugh,J., Cahill, L., Parent, M.B., Mesches, M.H., Coleman-Mesches, K., Salinas, J.A. (1995) Involvement of the amygdala in the regulation of memory storage. In: J. McGaugh, BermudezRattoni F. and Praco-Alcala R. A., eds. Plasticity in the Central Nervous System. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
  78. McGaugh, J.L., Castellano, C., and Brioni, J. (1990) Picrotoxin enhances latent extinction of conditioned fear. Behvioral Neuroscience 104: 264–267.CrossRefGoogle Scholar
  79. McIntosh, A.R. and Gonzalez-Lima, F. (1995) Functional network interactions between parallel auditory pathways during Pavlovian conditioned inhibition. Brain Res 683: 228–241.PubMedCrossRefGoogle Scholar
  80. McNish, K.A., Gewirtz, J.C. and Davis, M. (1997) Evidence of contextual fear conditioning following lesions of the hippocampus: A disruption of freezing but not fear-potentiated startle. J Neurosci 17: 9353–9360.Google Scholar
  81. Miserendino, M.J.D., Sananes,C.B., Melia, K.R., Davis, M. (1990) Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716–718.PubMedGoogle Scholar
  82. Morgan, M.A. and LeDoux, J.E. (1995) Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 109: 681–688.PubMedCrossRefGoogle Scholar
  83. Morgan, M.A. and LeDoux, J.E. (1996) Medial prefrontal cortex (mPFC) and the extinction of fear: Differential effecs of pre-or post-training lesions. Soc Neurosci Abst 22: 1116.Google Scholar
  84. Morgan, M.A. and LeDoux JE (1999) Contribution of ventrolateral prefrontal cortex to the acquistion and extinction of conditioned fear in rats. Neurobiol Learn Memory 72: 244–251.CrossRefGoogle Scholar
  85. Morgan, M.A., Romanski, L.M., LeDoux, J.E. (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Letts 163: 109–113.CrossRefGoogle Scholar
  86. Morrow, B.A., Elsworth, J.D., Inglis, F.M., Roth, R.H. (1999a) An antisense oligonucleotide reverses the footshock-induced expression of Fos in the rat medial prefrontal cortex and the subsequent expression of conditioned fear-induced immobility. J Neurosci 19: 5666–5673.PubMedGoogle Scholar
  87. Morrow, B.A., Elsworth, J.D., Rasmusson, A.M., Roth, R.H. (1999b) The role of mesoprefrontal dopamine neurons in the acquisition and expression of conditioned fear in the rat. Neuroscience 92: 553–564.PubMedCrossRefGoogle Scholar
  88. Nader, K. and LeDoux, J.E. (1999) Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. Behav Neurosci 113: 891–901.PubMedCrossRefGoogle Scholar
  89. Papini, M.R. and Bitterman, M.E. (1993) The two-test strategy in the study of inhibitory conditioning. Journal of Experimental Psychology: Animal Behavior Processes 19: 342–352.Google Scholar
  90. Pavlov, I.P. (1927) Conditioned Reflexes. Oxford University Press: Oxford University Press.Google Scholar
  91. Quirk, G.J., Kohanski, G.J., Ayala, O. (1998) Lesions of medial prefrontal cortex retard extinction of fear conditioning between sessions, but not within a session. Soc Neurosci Abst 28: 1683.Google Scholar
  92. Quirk, G.J., Rosaly, E., Romero, R.V., Santini, E., Muller, R.U. (1999) NMDA receptors are required for long-term but not short-term memory of extinction learning. Soc Neurosci Abst 25: 1620.Google Scholar
  93. Reiss, S. and Wagner, A.R. (1972) CS habituation produces a “latent inhibition effect” but no active “conditioned inhibition.” Learning Motivation 3: 237–245.Google Scholar
  94. Rescorla, R.A. (1969) Pavlovian conditioned inhibition. Psychological Bulletin 72: 77–94.CrossRefGoogle Scholar
  95. Rescorla, R.A. and Heth, C.D. (1975) Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychlogy: Animal Behavior Processes 1: 88–96.Google Scholar
  96. Robinson, G.B., Port, R.L., Stillwell, E.J. (1993) Latent inhibition of the classically conditioned rabbit nictitating membrane response is unaffected by the NMDA antagonist MK801. Psychobiology: 120124.Google Scholar
  97. Schmaltz, L.W. and Theiosus, J. (1972) Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (oryctolagus cuniculus). J Comp Physiol Psychol 79: 328–333.PubMedCrossRefGoogle Scholar
  98. Skinner, B. F. (1950) Are theories of learning necessary? Psychology Review 57: 193–216.CrossRefGoogle Scholar
  99. Skinner, B.F. (1938) Behavior of Organisms. New York: Appleton-Century-Crofts.Google Scholar
  100. Solomon, P.R. (1977) Role of hippocampus in blocking and conditioned inhibition of the rabbit’s nictitating membrane response. Journal of Comparative Physiological Psychiatry 91: 407–417.CrossRefGoogle Scholar
  101. Taylor, J.R. and Robbins, T.W. (1984) Enhanced behavioral control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology 84: 405–412.PubMedCrossRefGoogle Scholar
  102. Teich, A.H., McCabe, P.M., Gentile, C.C., Schneiderman, L.S., Winters, R.W., Liskosky, D.R., Schneiderman, N. (1989) Auditory cortex lesions prevent the extinction of heart rate conditioning to tonal stimuli in rabbits. Brain Res 480: 210–218.PubMedCrossRefGoogle Scholar
  103. Thomas, E., Yadin, E., Strickland, C.E. (1991) Septal unit activity during classical conditioning: A regional comparison. Brain Res 547: 303–308.Google Scholar
  104. Walker, D.L., Cassella, J.V., Lee, Y., de Lima, T.C.M., Davis, M. (1997) Opposing roles of the amygdala and dorsolateral periaqueductal gray in fear-potentiated startle. Brain Res Bull 111: 692702.Google Scholar
  105. Williams, D.A., Overmier, J.B., LoLordo, V.M. (1992) A reevaluation of Rescorla’s early dictums about Pavlovian Conditioned Inhibition. Psychological Bulletin 111: 275–290.CrossRefGoogle Scholar
  106. Willick, M.L. and Kokkinides, L. (1995) Cocaine enhances the expression of fear-potentiated startle: Evaluation of state-dependent extinction and the shock-sensitization of acoustic startle. Behav Neurosci 109: 929–938.Google Scholar
  107. Wilson, A., Brooks, D., and Bouton, M.E. (1995) The role of the rat hippocampal system in several effects of context extincition. Behav Neurosci 109: 828–836.PubMedCrossRefGoogle Scholar
  108. Yadin, E. (1989) Unit activity in the medial septum during differential appetitive conditioning. Behavioural Brain Research 33: 45–50.PubMedCrossRefGoogle Scholar
  109. Yadin, E. and Thomas, E. (1981) Septal correlates of conditioned inhibition. J Comp Physiol Psycho) 95: 331–340.CrossRefGoogle Scholar
  110. Yadin, E. and Thomas, E. (1996) Stimulation of the lateral septum attenuates immobilization-induced stress ulcers. Physiol Behav 59: 883–886.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Michael Davis
  • William A. Falls
  • Jonathan Gewirtz

There are no affiliations available

Personalised recommendations