Dissociation of associative and nonassociative concomitants of classical fear conditioning in the freely behaving rat.
Abstract
An acoustic stimulus previously paired with footshock elicits stereotyped increases in arterial pressure and heart rate and induces freezing behavior in freely behaving rats. Although the arterial pressure and freezing responses differ between groups given paired and random presentations of the tone and shock, the increases in heart rate do not. These observations, if taken at face value, suggest that the arterial pressure and freezing responses reflect associative learning but that the heart rate change is a nonassociative or a pseudoconditioned response. In this article we describe three experiments aimed at determining why the CS elicits similar increases in heart rate in groups given paired and random training. The first study demonstrates that regardless of the pseudoconditioning control procedure used (random, backwards, shock-alone, or naive), the same pattern of results is obtained: the increases in arterial pressure are greater in the paired than in each control group, but the heart rate rises to the same extent in all groups. The second study determined that the context in which the responses are tested (conditioning apparatus vs. novel test chamber) does not affect the general pattern of results obtained. The third study demonstrates that the superficially similar increases in heart rate in conditioned and pseudoconditioned rats are achieved by different physiological mechanisms: coactivation of the sympathetic and parasympathetic nervous systems in conditioned rats and sympathetic excitation alone in pseudoconditioned rats. Thus, the heart is influenced by associative emotional processes, but heart rate is not, under these conditions, a particularly useful index of those influences.
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When rats were conditioned to expect an electric shock, unrestrained compared to restrained rats showed greater sympathetic arousal and lower blood pressure reactivity prior to an electric shock.
“Iwata and LeDoux (1988) found that when rats were conditioned to expect an electric shock, their physiological responses changed based on whether they were unrestrained (and escape was presumably possible) versus restrained (with no possibility of escape). Unrestrained compared to restrained rats showed greater sympathetic arousal and lower blood pressure reactivity prior to an electric shock,”
From More than a feeling: A unified view of stress measurement for population science (2018) · cites this paper as Iwata and LeDoux, 1988
Cites
Falk, J. L. (1973) · Contemporary Psychology · doi:10.1037/0011818 · Cited by 2,288 · see citing works
Pavlovian conditioning and its proper control procedures.
Rescorla, R. A. (1967) · Psychological Review · doi:10.1037/h0024109 · Cited by 1,369 · see citing works
Some quantitative properties of anxiety.
Estes, W. K., & Skinner, B. F. (1941) · Journal of Experimental Psychology · doi:10.1037/h0062283 · Cited by 1,350 · see citing works
Conditioning and Associative Learning
Hill, W. F., & Mackintosh, N. J. (1984) · The American Journal of Psychology · doi:10.2307/1422540 · Cited by 1,323 · see citing works
Crouching as an index of fear.
Blanchard, R. J., & Blanchard, D. C. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0026779 · Cited by 1,077 · see citing works
Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit
Kapp, B. S., Frysinger, R. C., Gallagher, M., & Haselton, J. R. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90304-4 · Cited by 590 · see citing works
LeDoux, J., Sakaguchi, A., & Reis, D. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-03-00683.1984 · Cited by 532 · see citing works
Self-citationLeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902420204 · Cited by 530 · see citing works
Self-citationNeural mechanisms of learning and memory
(1992) · Chemico-Biological Interactions · doi:10.1016/0009-2797(92)90095-3 · Cited by 472 · see citing works
Individual Differences in Autonomic Response: Conditioned Association or Conditioned Fear?
Hodes, R. L., Cook, E. W., & Lang, P. J. (1985) · Psychophysiology · doi:10.1111/j.1469-8986.1985.tb01649.x · Cited by 355 · see citing works
Conditioned fear assessed by freezing and by the suppression of three different baselines
Bouton, M. E., & Bolles, R. C. (1980) · Animal Learning & Behavior · doi:10.3758/bf03199629 · Cited by 348 · see citing works
THE LAW OF INITIAL VALUE IN NEUROLOGY AND PSYCHIATRY: Facts and Problems1
WILDER, J. (1957) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-195701000-00009 · Cited by 339 · see citing works
Iwata, J., LeDoux, J. E., Meeley, M. P., Arnerić, S. P., & Reis, D. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)90020-x · Cited by 279 · see citing works
Self-citationLeDoux, J. E., Sakaguchi, A., Iwata, J., & Reis, D. J. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90034-5 · Cited by 207 · see citing works
Self-citationMind and brain: Dialogues in cognitive neuroscience
LeDoux, J. E., & Hirst, W. C. (1986) · DigitalGeorgetown (Georgetown University Library) · Cited by 163 · see citing works
Self-citationMcCarty, R. C., & Kopin, I. J. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90365-x · Cited by 134 · see citing works
LeDoux, J. E., Iwata, J., Pearl, D., & Reis, D. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)90383-5 · Cited by 117 · see citing works
Self-citationIwata, J., LeDoux, J. E., & Reis, D. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)91055-3 · Cited by 108 · see citing works
Self-citationInteractions between behavior and the cardiovascular system.
Cohen, D. H., & Obrist, P. A. (1975) · Circulation Research · doi:10.1161/01.res.37.6.693 · Cited by 107 · see citing works
Simple Method for CER Conditioning and Measurement
Leaf, R. C., & Muller, S. A. (1965) · Psychological Reports · doi:10.2466/pr0.1965.17.1.211 · Cited by 99 · see citing works
Gonzalez-Lima, F., & Scheich, H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91009-7 · Cited by 76 · see citing works
DiCara, L. V., Braun, J. J., & Pappas, B. A. (1970) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0030200 · Cited by 70 · see citing works
Vagal compensatory adjustment: Relationship to heart rate classical conditioning in rabbits.
Schneiderman, N., Dercar, D. H. V., Yehle, A. L., Manning, A. A., Golden, T., & Schneiderman, E. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0027514 · Cited by 69 · see citing works
Spontaneously hypertensive rats: Adrenergic hyperresponsivity to anticipation of electric shock
McCarty, R. C., Chiueh, C. C., & Kopin, I. J. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)91766-2 · Cited by 61 · see citing works
Limbic and Autonomic Nervous Systems Research
Dicara, L. (2011) · Springer US · doi:10.1007/978-1-4613-4407-0 · Cited by 58 · see citing works
LeDoux, J. E., Sakaguchi, A., & REIS, D. J. (1982) · Hypertension · doi:10.1161/01.hyp.4.6.853 · Cited by 58 · see citing works
Self-citationThe Neural Pathways and Informational Flow Mediating a Conditioned Autonomic Response
Cohen, D. H. (1974) · Springer eBooks · doi:10.1007/978-1-4613-4407-0_7 · Cited by 53 · see citing works
Trace and delayed heart-rate conditioning in rats as a function of US intensity.
Fitzgerald, R. D., & Teyler, T. J. (1970) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0028723 · Cited by 52 · see citing works
Heart rate conditioning in the rat
Fehr, F. S., & Stern, J. A. (1965) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(65)90086-3 · Cited by 51 · see citing works
CLASSICAL CONDITIONING OF HEART RATE AND GALVANIC SKIN RESPONSE IN THE RAT
Holdstock, T. L., & Schwartzbaum, J. S. (1965) · Psychophysiology · doi:10.1111/j.1469-8986.1965.tb02631.x · Cited by 49 · see citing works
Influence of vagal activity on classically conditioned heart rate in rats.
Fitzgerald, R. D., Martin, G. K., & O’Brien, J. H. (1973) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0034656 · Cited by 39 · see citing works
Heart rate and somatomotor activity in rats during signalled escape and yoked classical conditioning
Martin, G. K., & Fitzgerald, R. D. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90116-x · Cited by 32 · see citing works
(2004) · JAMA · doi:10.1001/jama.292.15.1891 · Cited by 32 · see citing works
Fitzgerald, R. D., Vardaris, R. M., & Brown, J. S. (1966) · Psychonomic Science · doi:10.3758/bf03330975 · Cited by 31 · see citing works
Peripheral autonomic mechanisms and Pavlovian conditioning in the rabbit (Oryctolagus cuniculus).
Albiniak, B. A., & Powell, D. A. (1980) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077747 · Cited by 30 · see citing works
Classical heart rate conditioning in the rat
McDonald, D. G., Stern, J. A., & Hahn, W. W. (1963) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(63)90022-9 · Cited by 26 · see citing works
Conditioning of Fear: A Function of the Delay of Reinforcement
Davitz, J. R., Mason, D. J., Mowrer, O. H., et al. (1957) · The American Journal of Psychology · doi:10.2307/1419231 · Cited by 21 · see citing works
Heart rate conditioning as a function of interstimulus interval in rats
Black, R. W., & Black, P. E. (1967) · Psychonomic Science · doi:10.3758/bf03331630 · Cited by 20 · see citing works
Duncan, P. M. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033319 · Cited by 20 · see citing works
A Psychobiological Perspective on the Cardiovascular System
Obrist, P., Lawler, J., & Gaebelein, C. (1974) · Springer eBooks · doi:10.1007/978-1-4613-4407-0_9 · Cited by 17 · see citing works
Hoffman, J. W., & Fitzgerald, R. D. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90012-4 · Cited by 14 · see citing works
Heart-Rate Conditioning in Rats as a Function of Interstimulus Interval
Fitzgerald, R. D., & Martin, G. K. (1971) · Psychological Reports · doi:10.2466/pr0.1971.29.3f.1103 · Cited by 14 · see citing works
Cunningham, C. L., Fitzgerald, R. D., & Francisco, D. L. (1977) · Animal Learning & Behavior · doi:10.3758/bf03214068 · Cited by 11 · see citing works
The reinforcing effects of vagal stimulation on classically conditioned heart rate in rats
Fitzgerald, R. D., & Hoffman, J. W. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90114-1 · Cited by 9 · see citing works
Cholinergic and adrenergic control of heart-rate changes in the rabbit
Kazis, E., Duncan, S., & Powell, D. A. (1974) · Bulletin of the Psychonomic Society · doi:10.3758/bf03333387 · Cited by 6 · see citing works
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Ulrich-Lai, Y. M., & Herman, J. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2647 · Cited by 3,318 · see citing works
POSNER, J., RUSSELL, J. A., & PETERSON, B. S. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050340 · Cited by 2,602 · see citing works
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Barrett, L. F., Adolphs, R., Marsella, S., Martinez, A. M., & Pollak, S. D. (2019) · Psychological Science in the Public Interest · doi:10.1177/1529100619832930 · Cited by 1,748 · see citing works
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Barrett, L. F. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw154 · Cited by 1,426 · see citing works
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Epel, E. S., Crosswell, A. D., Mayer, S. E., Prather, A. A., Slavich, G. M., Puterman, E., & Mendes, W. B. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.03.001 · Cited by 1,077 · see citing works
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Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
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Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991) · Psychological Review · doi:10.1037/0033-295x.98.4.459 · Cited by 819 · see citing works
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Roelofs, K. (2017) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2016.0206 · Cited by 616 · see citing works
Kozlowska, K., Walker, P., McLean, L., & Carrive, P. (2015) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000065 · Cited by 468 · see citing works
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.2.296 · Cited by 430 · see citing works
Barrett, L. F. (2009) · Cognition and Emotion · doi:10.1080/02699930902985894 · Cited by 371 · see citing works
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(1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61880-4 · Cited by 364 · see citing works
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BERNTSON, G. G., CACIOPPO, J. T., QUIGLEY, K. S., & FABRO, V. T. (1994) · Psychophysiology · doi:10.1111/j.1469-8986.1994.tb01024.x · Cited by 289 · see citing works
Frysztak, R. J., & Neafsey, E. J. (1994) · Brain Research · doi:10.1016/0006-8993(94)90024-8 · Cited by 245 · see citing works
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Barrett, L. F., & Satpute, A. B. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2017.07.045 · Cited by 180 · see citing works
Mendes, W. B. (2010) · Emotion Review · doi:10.1177/1754073910364149 · Cited by 70 · see citing works
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- Authors
- Iwata, J., & LeDoux, J. E.
- Affiliations
- Cornell University (US)
- ORCID
- LeDoux, Joseph E.
- Venue
- Behavioral Neuroscience
- Published
- 1988
- Volume
- 102
- Issue
- 1
- Pages
- 66-76
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W2022269251
- Cited by
- 194
- References
- 45
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 9 · 2023: 1 · 2022: 3 · 2021: 7 · 2020: 5 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 4 · 2015: 4 · 2014: 3 · 2013: 5 · 2012: 4
- FWCI
- 10.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL-18794)
- National Institute of Mental Health (MH38774)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- classical fear conditioning, pseudoconditioning, heart rate, arterial pressure, freezing behavior, acoustic stimulus, footshock, sympathetic nervous system, parasympathetic nervous system, associative learning, non-associative learning, emotional arousal
- MeSH terms
- Animals, Association Learning, Blood Pressure, Conditioning, Classical, Fear, Heart Rate, Learning, Male, Pulse, Rats, Inbred Strains, Reference Values, Rats
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