Conditioning pp 581-599 | Cite as

The Amygdala Central Nucleus: Contributions to Conditioned Cardiovascular Responding during Aversive Pavlovian Conditioning in the Rabbit

  • Bruce S. Kapp
  • Michela Gallagher
  • Craig D. Applegate
  • Robert C. Frysinger
Part of the Advances in Behavioral Biology book series (ABBI, volume 26)


The research described represents an attempt to determine the exact amygdala components which contribute to the acquisition of conditioned responding during aversive conditioning. Our initial analysis focuses on the amygdala central nucleus and its contribution to the acquisition of conditioned bradycardia during Pavlovian fear conditioning in the rabbit. The results demonstrate that (a) lesions of the central nucleus attenuate the magnitude of the conditioned bradycardia response, (b) the administration of ß-adrenergic antagonists and opiate agonists into the region of the central nucleus also attenuate the magnitude of the conditioned bradycardia response, (c) the medial component of the central nucleus projects directly to cardioregulatory nuclei in the dorsal medulla including the site of origin of cardioinhibitory neurons in the rabbit, (d) electrical stimulation of the central nucleus in rabbit produces profound, short-latency bradycardia and depressor responses, with maximum bradycardia elicited from the site of origin of the central nucleus-dorsal medulla projection, and (e) during the course of the conditioning procedure increases in central nucleus neuronal activity develop to the conditioned stimulus (CS) at the time when the conditioned bradycardia response develops. In some cases the magnitude of the increase in neuronal activity to the CS was significantly correlated with the magnitude of the bradycardia response to the CS over the course of the conditioning session.

The results are consistent with the hypothesis that at least one function of the amygdala central nucleus in the acquisition of conditioned bradycardia may be in the motoric expression of the conditioned response to the CS by modulation of vagal preganglionic cardioinhibitory neurons within the dorsal medulla.


Condition Stimulus Central Nucleus Pavlovian Conditioning Aversive Conditioning Dorsal Motor Nucleus 
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.


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  1. 1.
    G. Goddard, Functions of the amygdala, Psychol. Bull. 62: 89 (1964).CrossRefGoogle Scholar
  2. 2.
    N. J. Russo, B. S. Kapp, B. K. Holmquist, and R. E. Musty, Passive avoidance and amygdala lesions: Relationship with pituitary-adrenal system, Physiol. Behay. 16: 191 (1976).Google Scholar
  3. 3.
    A. A. Spevack, C. T. Campbell, and L. Drake, Effect of amygdalectomy on habituation and CER in rats, Physiol. Behay. 15: 199 (1975).Google Scholar
  4. 4.
    P. G. Henke, Effects of reinforcement omission on rats with lesions in the amygdala, J. Comp. Physiol. Psych. 84: 187 (1973).CrossRefGoogle Scholar
  5. 5.
    D. C. Blanchard and R. J. Blanchard, Innate and conditioned reactions to threat in rats with amygdaloid lesions, J. Comp. Physiol. Psych. 81: 281 (1972).Google Scholar
  6. 6.
    T. Werka, J. Skär, and H. Ursin, Exploration and avoidance in rats with lesions in amygdala and piriform cortex, J. Comp. Physiol. Psych. 92: 672 (1978).CrossRefGoogle Scholar
  7. 7.
    M. McIntyre and D. G. Stein, Differential effects of one vs. two stage amygdaloid lesions on activity, exploratory and avoidance behavior in the albino rat, Behay. Biol. 9: 451 (1973).Google Scholar
  8. 8.
    S. P. Grossman, L. Grossman, and L. Walsh, Functional organization of the rat amygdala with respect to avoidance behavior, J. Comp. Physiol. Psych. 88: 829 (1975).CrossRefGoogle Scholar
  9. 9.
    S. M. Hilton and A. W. Zbrozyna, Amygdaloid region for defense reactions and its efferent pathway to the brain stem, J. Physiol. 165: 160 (1963).PubMedGoogle Scholar
  10. 10.
    E. Roldan, R. Alvarez-Pelaez, and A. Fernandez deMolina, Electrographic study of the amygdaloid defense response, Physiol. Behay. 13: 779 (1974).Google Scholar
  11. 11.
    G. Stock, K. H. Schlör, H. Heidt, and J. Buss, Psychomotor behaviour and cardiovascular patterns during stimulation of the amygdala, Pflügers Archiv. 376: 177 (1978).PubMedCrossRefGoogle Scholar
  12. 12.
    H. Ursin and B. R. Kaada, Functional localization within the amygdaloid complex in the cat, EEG Clin. Neurophysiol. 12: 1 (1960).Google Scholar
  13. 13.
    D. A. Hopkins and G. Holstege, Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat, Exp. Brain Res., 32: 529 (1978).Google Scholar
  14. 14.
    V. C. Abrahams, S. M. Hilton, and A. Zbrozyna, Active muscle vasodilation produced by stimulation of the brain stem. Its significance in the defense reaction, J. Physiol., 154: 491 (1960).PubMedGoogle Scholar
  15. 15.
    J. H. Coote, S. M. Hilton, and A. W. Zbrozyna, The ponto-medullary area integrating the defense reaction in the cat and its influence on muscle blood flow, J. Physiol. 229: 257 (1973).PubMedGoogle Scholar
  16. 16.
    A. Fredericks, J. W. Moore, F. U. Metcalf, J. S. Schwaber, and N. Schneiderman, Selective autonomic blockade of conditioned and unconditioned heart rate changes in rabbits, Pharm. Biochem. Behay. 2: 493 (1974).Google Scholar
  17. 17.
    D. A. Powell and E. Kazis, Blood pressure and heart rate changes accompanying classical eyeblink conditioning in the rabbit (Oryctolagus C,uniculus), Psychophysiol. 13: 441 (1976).CrossRefGoogle Scholar
  18. 18.
    N. Schneiderman, D. H. VanDercar, A. L. Yehle, A. A. Manning, T. Golden, and E. Schneiderman, Vagal compensatory adjustment: Relationship to heart rate classical conditioning in rabbits, J. Comp. Physiol. Psych. 68: 175 (1969).Google Scholar
  19. 19.
    D. H. Cohen, Involvement of avian amygdala homolog (archistriatum posterior and mediale) in defensively conditioned heart rate change, J. Comp. Neurol. 160: 13 (1975).Google Scholar
  20. 20.
    V. Frisch, HerzFrequenzänderung bei Druckreaktion junger Nestflucher, Z. Tierpsychol. 23: 497 (1966).Google Scholar
  21. 21.
    B. S. Kapp, R. C. Frysinger, M. Gallagher, and J. Haselton, Amygdala central nucleus lesions: Effects on heart rate conditioning in the rabbit, Physiol. Behay. 23: 1109 (1979).CrossRefGoogle Scholar
  22. 22.
    J. H. Fallon, D. A. Koziell, and R. Y. Moore, Catecholamine innervation of the basal forebrain. II. Amygdala, suprahinal cortex and entorhinal cortex, J. Comp. Neurol. 180: 509 (1978).Google Scholar
  23. 23.
    V. M. Pickel, M. Segal, and F. E. Bloom, A radiographic study of the efferent pathways of the nucleus locus coeruleus, J. Comp. Neurol. 155: 15 (1974).Google Scholar
  24. 24.
    M. Gallagher, B. S. Kapp, R. E. Musty, and P. A. Driscoll, Memory formation: Evidence for a specific neurochemical system in the amygdala, Science 198: 423 (1977).PubMedCrossRefGoogle Scholar
  25. M. Gallagher, B. S. Kapp, R. C. Frysinger, and P. R. Rapp, 8-adrenergic manipulation in amygdala central nucleus alters rabbit heart rate conditioning, Pharm. Biochem. Behay. 12:419 (1980).Google Scholar
  26. 26.
    D. B. Bylund and S. H. Snyder, Biochemical identification of the ß-adrenergic receptor in mammalian brain, Mol. Pharm. 12: 1279 (1976).Google Scholar
  27. 27.
    J. L. Martinez. L. McGaugh (Eds.), Endogenous Peptides and Learning and Memory Processes, Academic Press, New York (1981).Google Scholar
  28. 28.
    M. Gallagher and B. S. Kapp, Manipulation of opiate activity in the amygdala alters memory processes, Life Sci. 23: 1973 (1978).PubMedCrossRefGoogle Scholar
  29. 29.
    C. Gros, P. Pradelles, J. Humbert, F. Dray, G. Le Gal La Salle, and Y. Ben-Ari, Regional distribution of met-enkephalin within the amygdaloid complex and bed nucleus of the stria terminalis, Neuro. Lett. 10: 193 (1978).Google Scholar
  30. 30.
    R. Simantov, M. G. Kuhar, G. R. Uhl, and S. H. Snyder, Opioid peptide enkephalin: Immunohistochemícal mapping in rat central nervous system, Proc. Natl. Acad. Sci. U.S.A. 74: 2167 (1977).CrossRefGoogle Scholar
  31. 31.
    R. R. Goodman, S. H. Snyder, M. J. Kuhar, and W. S. Young III, Differentiation of delta and mu opiate receptor localizations by light microscopic autoradiography, Proc. Natl. Acad. Sci. U.S.A. 77: 6239 (1980)CrossRefGoogle Scholar
  32. 32.
    M. Gallagher, B. S. Kapp, C. L. McNall, and J. P. Pascoe, Opiate effects in the amygdala central nucleus on heart rate conditioning in rabbits, Pharm. Biochem. Behay. 14: 497 (1981).Google Scholar
  33. 33.
    R. J. Rodgers, Influence of intra-amygdaloid opiate injection on shock thresholds, tail flick latencies and open field behavior in rats, Brain Res. 153: 211 (1978).PubMedCrossRefGoogle Scholar
  34. 34.
    A. Goldstein, G. T. Pryor, L. S. Otis, and F. Larsen, On the role of endogenous opioid peptides: Failure of naloxone to influence shock escape threshold in the rat, Life Sci. 18: 599 (1976).Google Scholar
  35. 35.
    S. E. File and R. J. Rodgers, Partial anxiolytic action of morphine sulfate following microinjection into the central nucleus of the amygdala in rats, Pharm. Biochem. Behay. 11: 313 (1979).Google Scholar
  36. 36.
    J. S. Schwaber, and N. Schneiderman, Aortic nerve activated cardioinhibitory neurons and interneurons, A. J. Physiol. 299: 783 (1975).Google Scholar
  37. 37.
    J. S. Schwaber, B. S. Kapp, and G. Higgins, The origin and extent of direct amygdala projections to the region of the dorsal motor nucleus of the vagus and the nucleus of the solitary tract, Neuro. Lett. 20: 15 (1980).Google Scholar
  38. 38.
    J. S. Schwaber, B. S. Kapp, G. A. Higgins, and P. R. Rapp, The origin, extent and terminal distribution of direct amygdala central nucleus projections to the dorsal motor nucleus and nucleus of the solitary tract, Neuro. Abs. 6: 816 (1980).Google Scholar
  39. 39.
    B. S. Kapp, M. Gallagher, M. D. Underwood, C. L. McNall, and D. Whitehorn, Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit, Submitted, Brain Res. (1981).Google Scholar
  40. B. S. Kapp, C. D. Applegate, M. D. Underwood, and C. L. McNall, Electrical stimulation of the amygdala central nucleus in the awake rabbit: Effects on heart rate, respiration and somatomotor behavior, Neuro. Abs. 7 (1981).Google Scholar
  41. C. D. Applegate, R. C. Frysinger, B. S. Kapp, and M. Gallagher, Neuronal activity recorded from the amygdala central nucleus during aversive Pavlovian heart rate conditioning in the rabbit, Neuro. Abs. 7 (1981).Google Scholar
  42. 42.
    J. S. Schwartzbaum and J. R. Morse, Taste responsivity of amygdaloid units in behaving rabbits: A methodological report, Brain Res. Bull. 3: 131 (1978).CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1982

Authors and Affiliations

  • Bruce S. Kapp
    • 1
  • Michela Gallagher
    • 2
  • Craig D. Applegate
    • 1
  • Robert C. Frysinger
    • 1
  1. 1.Department of PsychologyUniversity of VermontBurlingtonUSA
  2. 2.Department of PsychologyUniversity of North CarolinaChapel HillUSA

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