Effects of extinction on classical conditioning and conditioning-specific reflex modification of rabbit heart rate

Behavioural Brain Research

Volumn 206, Issue 1, 2010, Pages 127-134

  Burhans, Lauren B ^a   Smith Bell, Carrie ^a   Schreurs, Bernard G ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Classical conditioning; Extinction; Fear conditioning; Heart rate conditioning; Rabbit; Reflex modification

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRADYCARDIA; CONDITIONED REFLEX; CONTROLLED STUDY; FEAR; HEART RATE; HEART STIMULATION; MALE; NONHUMAN; PRIORITY JOURNAL; RABBIT; REINFORCEMENT; VAGUS REFLEX;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; ELECTROCARDIOGRAPHY; EXTINCTION, PSYCHOLOGICAL; HEART RATE; MALE; RABBITS; REFLEX;

EID: 70350200852     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.09.007     Document Type: Article

References (80)

1. Albiniak B.A., and Powell D.A. Peripheral autonomic mechanisms and Pavlovian conditioning in the rabbit (Oryctolagus cuniculus). J Comp Physiol Psychol 94 (1980) 1101-1113
2. Antoniadis E.A., and McDonald R.J. Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 101 (1999) 1-13
3. Berlau D.J., and McGaugh J.L. Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basal amygdala. Neurobiol Learn Mem 86 (2006) 123-132
4. Berntson G.G., Hart S., and Sarter M. The cardiovascular startle response: anxiety and the benzodiazepine receptor complex. Psychophysiology 34 (1997) 348-357
5. Bradley D.J., Ghelarducci B., and Spyer K.M. The role of the posterior cerebellar vermis in cardiovascular control. Neurosci Res 12 (1991) 45-56
6. Buchanan S.L., and Thompson R.H. Mediodorsal thalamic lesions and Pavlovian conditioning of heart rate and eyeblink responses in the rabbit. Behav Neurosci 104 (1990) 912-918
7. Buck D.L., Seager M.A., and Schreurs B.G. Conditioning-specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response: generality and nature of the phenomenon. Behav Neurosci 115 (2001) 1039-1047
8. Burhans L.B., Smith-Bell C., and Schreurs B.G. Conditioning-specific reflex modification of the rabbit's nictitating membrane response and heart rate: behavioral rules, neural substrates, and potential applications to posttraumatic stress disorder. Behav Neurosci 122 (2008) 1191-1206
9. Carrive P. Conditioned fear to environmental context: cardiovascular and behavioral components in the rat. Brain Res 858 (2000) 440-445
10. Chachich M., and Powell D.A. Both medial prefrontal and amygdala central nucleus lesions abolish heart rate classical conditioning, but only prefrontal lesions impair reversal of eyeblink differential conditioning. Neurosci Lett 257 (1998) 151-154
11. Chang C.H., and Maren S. Early extinction after fear conditioning yields a context-independent and short-term suppression of conditional freezing in rats. Learn Mem 16 (2009) 62-68
12. Cohen D.H., and Pitts L.H. Vagal and sympathetic components of conditioned cardioacceleration in the pigeon. Brain Res 9 (1968) 15-31
13. Cohen H., Zohar J., Matar M.A., Zeev K., Loewenthal U., and Richter-Levin G. Setting apart the affected: the use of behavioral criteria in animal models of post traumatic stress disorder. Neuropsychopharmacology 29 (2004) 1962-1970
14. Coleman S.R., and Gormezano I. Classical conditioning of the rabbit's (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. J Comp Physiol Psychol 77 (1971) 447-455
15. Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol 61 (2006) 741-756
16. Duan Y.-F., Winters R.W., McCabe P.M., Green E.J., Huang Y., and Schneiderman N. Cardiorespiratory components of defense reaction elicited from paraventricular nucleus. Physiol Behav 61 (1997) 325-330
17. Dudeney J.E., Olsen K.N., and Kehoe E.J. Time-specific extinction and recovery of the rabbit's (Oryctolagus cuniculus) conditioned nictitating membrane response using mixed interstimulus intervals. Behav Neurosci 121 (2007) 808-813
18. Dykman R.A., and Gantt W.H. The parasympathetic component of unlearned and acquired cardiac responses. J Comp Physiol Psychol 52 (1959) 163-167
19. Fitzgerald R.D., Martin G.K., and O'Brien J.H. Influence of vagal activity on classical conditioned heart rate in rats. J Comp Physiol Psychol 83 (1973) 485-491
20. Ghelarducci B., and Sebastiani L. Role of the medial prefrontal cortex in the development of conditioned bradycardia in rabbits with lesions of the cerebellar vermis. Exp Brain Res 129 (1999) 185-190
21. Ghelarducci B., and Sebastiani L. Classical heart rate conditioning and affective behavior: the role of the cerebellar vermis. Arch Ital Biol 135 (1997) 369-384
22. Ginsberg J.P., Ayers E., Burriss L., and Powell D.A. Disruption of bradycardia associated with discriminative conditioning in combat veterans with PTSD. Neuropsychiatr Dis Treat 4 (2008) 635-646
23. Gormezano I. Classical conditioning. In: Sidowski J.B. (Ed). Experimental methods and instrumentation in psychology (1966), McGraw-Hill, New York 385-420
24. Gray A.L., Johnson T.A., Ardell J.L., and Massari V.J. Parasympathetic control of the heart. II. A novel intrinsic cardiac circuit mediates neural control of heart rate. J Appl Physiol 96 (2004) 2273-2278
25. Gruart A., and Yeo C.H. Cerebellar cortex and eyeblink conditioning: bilateral regulation of conditioned responses. Exp. Brain Res 104 (1995) 431-448
26. Hayes E., Pugsley M.K., Penz W.P., Adaikan G., and Walker M.J.A. Relationship between QaT and RR intervals in rats, guinea pigs, rabbits, and primates. J Pharmacol Toxicol Methods 32 (1994) 201-207
27. Heldt S.A., and Ressler K.J. Training-induced changes in the expression of GABAA-associated genes in the amygdala after the acquisition and extinction of Pavlovian fear. Eur J Neurosci 26 (2007) 3631-3644
28. Hofmann S.G. Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders. Clin Psychol Rev 28 (2008) 199-210
29. Iwata J., and LeDoux J.E. Dissociation of associative and nonassociative concomitants of classical fear conditioning in the freely behaving rat. Behav Neurosci 102 (1988) 66-76
30. Katcher A.H., Solomon R.L., Turner L.H., LoLordo V., Overmier J.B., and Rescorla R.A. Heart rate and blood pressure responses to signaled and unsignaled shocks: effects of cardiac sympathectomy. J Comp Physiol Psychol 68 (1969) 163-174
31. Kazis E., Milligan W.L., and Powell D.A. Autonomic-somatic relationships: blockade of heart rate and corneo-retinal potential responses. J Comp Physiol Psychol 84 (1973) 98-110
32. Kehoe E.J., and Macrae M. Classical conditioning of the rabbit nictitating membrane can be fast or slow: implications for Lennartz and Weinberger's (1992) two-factor theory. Psychobiology 22 (1994) 1-4
33. Kehoe E.J., and White N.E. Extinction revisited: similarities between extinction and reductions in US intensity in classical conditioning of the rabbit's nictitating membrane response. Anim Learn Behav 30 (2002) 96-111
34. Lennartz R.C., and Weinberger N.M. Analysis of response systems in Pavlovian conditioning reveals rapidly versus slowly acquired conditioned responses: support for two factors, implications for behavior and neurobiology. Psychobiology 20 (1992) 93-119
35. Leung H.T., and Westbrook R.F. Spontaneous recovery of extinguished fear responses deepens their extinction: a role for error-correction mechanisms. J Exp Psychol Anim Behav Process 34 (2008) 461-474
36. Mao S.C., Lin H.C., and Gean P.W. Augmentation of fear extinction by d-cycloserine is blocked by proteasome inhibitors. Neuropsychopharmacology 33 (2008) 3085-3095
37. McCabe P.M., Schneiderman N., Jarrell T.W., Gentile C.G., Teich A.H., Winters R.W., et al. Central pathways involved in classical differential conditioning of heart rate responses in rabbits. In: Gormezano I., and Wasserman E.A. (Eds). Learning and memory: the behavioral and biological substrates (1992), Lawrence Erlbaum Associates, Hillsdale, New Jersey 321-346
38. McEchron M.D., McCabe P.M., Green E.J., Llabre M.M., and Schneiderman N. Air puff versus shock unconditioned stimuli in rabbit heart rate conditioning. Physiol Behav 51 (1992) 195-199
39. McEchron M.D., Tseng W., and Disterhoft J.F. Neurotoxic lesions of the dorsal hippocampus disrupt auditory-cued trace heart rate (fear) conditioning in rabbits. Hippocampus 10 (2000) 739-751
40. McEchron M.D., Tseng W., and Disterhoft J.F. Single neurons in CA1 hippocampus encode trace interval duration during trace heart rate (fear) conditioning in rabbit. J Neurosci 23 (2003) 1535-1547
41. Myers K.M., and Davis M. Mechanisms of fear extinction. Mol Psychiatry 12 (2007) 120-150
42. Nijsen M.J., Croiset G., Diamant M., Stam R., Delsing D., deWied D., et al. Conditioned fear-induced tachycardia in the rat: vagal involvement. Eur J Pharmacol 350 (1998) 211-222
43. Nijsen M.J.M.A., Croiset G., Diamant M., de Wied D., and Wiegant V.M. CRH signalling in he bed nucleus of the stria terminalis is involved in stress-induced cardiac vagal activation in conscious rats. Neuropsychopharmacology 24 (2001) 1-10
44. Nolan B.C., and Freeman Jr. J.H. Purkinje cell loss by OX7-saporin impairs acquisition and extinction of eyeblink conditioning. Learn Mem 13 (2006) 359-365
45. Notterman J.M., Schoenfeld W.N., and Bersh P.J. A comparison of three extinction procedures following heart rate conditioning. J Abnorm Psychol 47 (1952) 675-677
46. Obrist P.A., Wood D.M., and Perez-Reyes M. Heart rate during conditioning in humans: effects of UCS intensity, vagal blockade, and adrenergic block of vasomotor activity. J Exp Psychol 70 (1965) 37-42
47. Pascoe J.P., and Kapp B.S. Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 16 (1985) 117-133
48. Pascoe J.P., Supple W.F., and Kapp B.S. Learning and memory: vertebrate models. In: Martinez J.L., and Kesner R.P. (Eds). Learning and memory: a biology view (1991), Academic Press, San Diego 359-407
49. Powell D.A., Churchwell J., and Burriss L. Medial prefrontal lesions and Pavlovian eyeblink and heart rate conditioning: effects of partial reinforcement on delay and trace conditioning in rabbits (Oryctolagus cuniculus). Behav Neurosci 119 (2005) 180-189
50. Powell D.A., and Ginsberg J.P. Single unit activity in the medial prefrontal cortex during Pavlovian heart rate conditioning: Effects of peripheral autonomic blockade. Neurobiol Learn Mem 84 (2005) 200-213
51. Powell D.A., and Levine-Bryce D. A comparison of two model systems of associative learning: heart rate and eyeblink conditioning in the rabbit. Psychophysiology 25 (1988) 672-682
52. Powell D.A., Watson K., and Maxwell B. Involvement of subdivisions of the medial prefrontal cortex in learned cardiac adjustments in rabbits. Behav Neurosci 108 (1994) 294-307
53. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008) 56-72
54. Raskin D.C. Orienting and defensive reflexes and conditioning. In: Black A.H., and Prokasy W.F. (Eds). Classical conditioning II: Current research and theory (1972), Appleton-Century-Crofts, New York 269-289
55. Raskin D.C., Kotses H., and Bever J. Autonomic indicators of orienting and defensive reflexes. J Exp Psychol 80 (1969) 423-433
56. Richter A., Schumann N.P., and Zweiner U. Characteristics of heart rate fluctuations and respiratory movements during orienting, passive avoidance and flight-fight behavior in rabbits. Int J Psychophysiol 10 (1990) 75-83
57. Robleto K., and Thompson R.F. Extinction of a classically conditioned response: red nucleus and interpositus. J Neurosci 28 (2008) 2651-2658
58. 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) 1254-1276
59. Schadt J.C., and Hasser E.M. Hemodynamic effects of acute stressors in the conscious rabbit. Am J Physiol Regul Integr Comp Physiol 274 (1998) R814-R821
60. Schneiderman N. Response system divergencies in aversive classical conditioning. In: Black A.H., and Prokasy W.F. (Eds). Classical conditioning II: Current research and theory (1972), Appleton-Century-Crofts, New York 341-376
61. Schneiderman N., Smith M.C., Smith A.C., and Gormezano I. Heart rate classical conditioning in rabbits. Psychon Sci 6 (1966) 241-242
62. Schneiderman N., Van Dercar D.H., Yehle A.L., Manning A.A., Golden T., and Schneiderman E. Vagal compensatory adjustment: relationship to heart rate classical conditioning in rabbits. J Comp Physiol Psychol 68 (1969) 175-183
63. Schreurs B.G. Classical conditioning and modification of the rabbit's (Oryctolagus cuniculus) unconditioned nictitating membrane response. Behav Cogn Neurosci Rev 2 (2003) 83-96
64. Schreurs B.G., and Alkon D.L. Learning and memory. In: Crockard A., Hayward R., and Hoff J.T. (Eds). Neurosurgery: the scientific basis of clinical practice, vol. 1 (1997), Blackwell Scientific, Oxford 192-204
65. Schreurs B.G., Crum J.M., Wang D., and Smith-Bell C.A. Conditioning-specific reflex modification of rabbit (Oryctolagus cuniculus) heart rate. Behav Neurosci 119 (2005) 1484-1495
66. Schreurs B.G., Gonzalez-Joekes J., and Smith-Bell C.A. Conditioning-specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response is sensitive to context. Learn Behav 34 (2006) 315-324
67. Schreurs B.G., Oh M.M., Hirashima C., and Alkon D.L. Conditioning-specific modification of the rabbit's unconditioned nictitating membrane response. Behav Neurosci 109 (1995) 24-33
68. Schreurs B.G., Shi T., Pineda III S., and Buck D.L. Conditioning the unconditioned response: modification of the rabbit's (Oryctolagus cuniculus) unconditioned nictitating membrane response. J Exp Psychol Anim Behav Process 26 (2000) 144-156
69. Schreurs B.G., and Smith-Bell C.A. Heart rate changes during conditioning-specific reflex modification of the rabbit's (Oryctolagus cuniculus) nictitating membrane response. Neurobiol Learn Mem 84 (2005) 148-158
70. Schreurs B.G., Smith-Bell C.A., Darwish D.S., Wang D., Burhans L.B., Gonzales-Joekes J., et al. Cholesterol enhances classical conditioning of the rabbit heart rate response. Behav Brain Res 181 (2007) 52-63
71. Schreurs B.G., Tomsic D., Gusev P.A., and Alkon D.L. Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. J Neurophysiol 77 (1997) 86-92
72. Schulz D., Huston J.P., Buddenberg T., and Topic B. "Despair" induced by extinction trials in the water maze: relationship with measures of anxiety in aged and adult rats. Neurobiol Learn Mem 87 (2007) 309-323
73. Seager M.A., Smith-Bell C.A., and Schreurs B.G. Conditioning-specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response: US intensity effects. Learn Behav 31 (2003) 292-298
74. Supple Jr. W.F., and Kapp B.S. The anterior cerebellar vermis: essential involvement in classically conditioned bradycardia in the rabbit. J Neurosci 13 (1993) 3705-3711
75. Weidemann G., and Kehoe E.J. Savings in classical conditioning in the rabbit as a function of extended extinction. Learn Behav 31 (2003) 49-68
76. Wikgren J., and Korhonen T. Interpositus nucleus inactivation reduces unconditioned response amplitude after paired but not explicitly unpaired treatment in rabbit eyeblink conditioning. Neurosci Lett 308 (2001) 181-184
77. Winters R.W., McCabe B.J., and Schneiderman N. Functional utility and neurobiology of conditioned autonomic responses. In: Moore J.W. (Ed). A neuroscientists guide to classical conditioning (2002), Springer-Verlag, New York 46-85
78. Yehle A., Dauth G., and Schneiderman N. Correlates of heart-rate classical conditioning in curarized rabbits. J Comp Physiol Psychol 64 (1967) 98-104
79. Yehle A.L. Divergences among rabbit response systems during three-tone classical discrimination conditioning. J Exp Psychol 77 (1968) 468-473
80. Zimny G.H., Stern J.A., and Fjeld S.P. Effects of CS and UCS relationships on electrodermal response and heart rate. J Exp Psychol 72 (1966) 177-181