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.

Falls, William A.; Davis, Michael

doi:10.1037/0735-7044.109.3.379

Cited by 110Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

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.

Falls, William A., Davis, Michael·1995·Behavioral Neuroscience

DOI 10.1037/0735-7044.109.3.379

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Abstract

Lesions of the amygdala block the expression of fear-potentiated startle following either moderate or extensive light + shock training. The present experiment assessed whether lesions of the amygdala would also block the expression of conditioned inhibition of fear. Rats were given conditioned inhibition training in which a light was paired with shock and a noise and light compound was presented in the absence of shock. Then half of the rats were given bilateral electrolytic lesions of the amygdala and the remaining rats were sham operated. Lesions of the amygdala blocked the expression of fear-potentiated startle to the light. To assess whether conditioned inhibition was disrupted, rats were retrained with light + shock pairings with no further conditioned inhibition training. Amygdala lesioned rats reacquired fear-potentiated startle to the light (Kim & Davis, 1993). Importantly, the noise conditioned inhibitor retained its ability to inhibit fear-potentiated startle to the retrained light. These results indicate that areas of the amygdala critical for initial performance of fear-potentiated startle are not critical for the expression of conditioned inhibition.

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The amygdala has been implicated in both threat learning and threat extinction processes.
“For thirty years, the amygdala has been implicated in both threat learning [48] and threat extinction [49] processes.”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [49]

Conditioned fear as revealed by magnitude of startle response to an auditory stimulus.
Brown, J. S., Kalish, H. I., & Farber, I. E. (1951) · Journal of Experimental Psychology · doi:10.1037/h0060166 · Cited by 637 · see citing works

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Suppressing fear in the presence of a safety cue requires infralimbic cortical signaling to central amygdala
Ng, K. H., Pollock, M., Escobedo, A., Bachman, B. B., Miyazaki, N. L., Bartlett, E. L., & Sangha, S. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01598-0 · Cited by 20 · see citing works
“In other safety conditioning studies, Falls and Davis [24] have previously investigated the role of the central amygdala in conditioned inhibition of a fear potentiated startle response by lesioning the CeA after training to a safety cue.”
Background
Anxiolytic-like Effects of the Neurokinin 1 Receptor Antagonist GR-205171 in the Elevated Plus-Maze and Contextual Fear-Potentiated Startle Model of Anxiety in Gerbils
Heldt, S. A., Davis, M., Ratti, E., Corsi, M., Trist, D., & Ressler, K. (2009) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32832ec594 · Cited by 20 · see citing works
“, 2007), and (iii) lesions of brain structures critical for the expression of fear eliminate the expression of FPS (Sananes and Davis, 1992; Campeau and Davis, 1995; Falls and Davis, 1995; Heldt et al., 2000).”
Self-citation
Inhibitory learning tests of conditioned stimulus associability in rats with lesions of the amygdala central nucleus.
Holland, P. C., Chik, Y., & Zhang, Q. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.5.1154 · Cited by 18 · see citing works
Destruction of the auditory thalamus disrupts the production of fear but not the inhibition of fear conditioned to an auditory stimulus.
Heldt, S. A., & Falls, W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)01047-6 · Cited by 18
Self-citation
Chronic inhibition of GABA synthesis in the infralimbic cortex facilitates conditioned safety memory and reduces contextual fear
Kreutzmann, J. C., & Fendt, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0788-8 · Cited by 16 · see citing works
Conditioned Inhibition of Fear and Reward in Male and Female Rats
Krueger, J. N., Patel, N. N., Shim, K., Ng, K. H., & Sangha, S. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107881 · Cited by 15 · see citing works
“Using a serial presentation design in which the inhibitor cue was followed by the fear cue, without shock delivery, Falls and Davis (Falls & Davis,1995) showed the CeA was not necessary for safety”
Method
Electrolytic lesions of the nucleus accumbens core (but not the medial shell) and the basolateral amygdala enhance context-specific locomotor sensitization to nicotine in rats.
Kelsey, J. E., Gerety, L., & Guerriero, R. (2009) · Behavioral Neuroscience · doi:10.1037/a0015573 · Cited by 14 · see citing works
The effect of long context exposure on cued conditioning and c-fos expression in the rat forebrain.
Pérez-Villalba, A., Teruel-Martí, V., Ruiz‐Torner, A., & Olucha-Bordonau, F. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.02.028 · Cited by 14 · see citing works
Medial dorsal thalamic lesions impair blocking and latent inhibition of the conditioned eyeblink response in rats.
Nicholson, D., & Jr. Freeman John, H. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.2.276 · Cited by 14 · see citing works
Posttraining lesions of the auditory thalamus, but not cortex, disrupt the inhibition of fear conditioned to an auditory stimulus
Heldt, S. A., & Falls, W. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04604.x · Cited by 13 · see citing works
Self-citation
Blockade of GABAA receptors in the interpositus nucleus modulates expression of conditioned excitation but not conditioned inhibition of the eyeblink response
Nolan, B. C., Nicholson, D., & Freeman, J. (2002) · Integrative Physiological & Behavioral Science · doi:10.1007/bf02734250 · Cited by 13
“A series of studies investigated the neural mechanisms underlying conditioned inhibition of the fear-potentiated startle response in rats (Falls, Bakken, & Heldt, 1997; Falls & Davis, 1995; Gewirtz, Falls, & Davis, 1997; Heldt, Falls, & Coover, 2000; Waddell, Pistell, Heldt, & Falls, 2000).”
Background
From safety to frustration: The neural substrates of inhibitory learning in aversive and appetitive conditioning procedures.
Cassaday, H., Muir, C., Stevenson, C., Bonardi, C., Hock, R., & Waite, L. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107757 · Cited by 12 · see citing works
“Negative or inconclusive evidence in aversively motivated procedures has also been reported following neonatal amygdala (Kazama et al., 2012) and CeA lesions (Falls & Davis, 1995).”
Background
Posttraining lesion of the superior colliculus interferes with feature-negative discrimination of fear-potentiated startle.
Waddell, J., Heldt, S. A., & Falls, W. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00405-9 · Cited by 12 · see citing works
Self-citation
Neurobiological Relationships Between Ambient Lighting and the Startle Response to Acoustic Stress in Humans
Basso, M. R. (2001) · International Journal of Neuroscience · doi:10.3109/00207450108986542 · Cited by 12 · see citing works
Understanding the Causes of Reduced Startle Reactivity in Stress-Related Mental Disorders
Beck, K., & Catuzzi, J. E. (2013) · InTech eBooks · doi:10.5772/53066 · Cited by 10 · see citing works
“The amygdala is predominately associated with causing classically conditioned fear-potentiated ASRs [5], and, in fact, has been specifically shown not to have a role in startle inhibition, at least via a learned condi‐ tioned inhibitor [6].”
Background
Modulation of the magnitude of conditioned taste aversion in rats with excitotoxic lesions of the basolateral amygdala
Molero-Chamizo, A. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.11.009 · Cited by 10
“…CTA and in the visceral processing during CTA has been related to the efferents of the basolateral amygdala to the central nucleus (Inui, Inui-Yamamoto, Yoshioka, Ohzawa, & Shimura, 2013) and the ability of the central nucleus to process visceral information (Agüera & Puerto, 2015), respectively.”
Hippocampal Involvement in Safety Signal Learning Varies With Anxiety Among Healthy Adults
Odriozola, P., Kribakaran, S., Cohodes, E. M., Zacharek, S. J., McCauley, S., Haberman, J. T., Quintela, L. A., Hernandez, C., Spencer, H., Pruessner, L., et al. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.05.007 · Cited by 7 · see citing works
Extended fear conditioning reveals a role for both N-methyl-d-aspartic acid and non-N-methyl-d-aspartic acid receptors in the amygdala in the acquisition of conditioned fear
Pistell, P. J., & Falls, W. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.012 · Cited by 4 · see citing works
Self-citation
Auditory stimuli suppress contextual fear responses in safety learning independent of a possible safety meaning
Mombelli, E., Osypenko, D., Palchaudhuri, S., Sourmpis, C., Brea, J., Kochubey, O., & Schneggenburger, R. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1415047 · Cited by 2
Translational Approaches to the Neurobiological Study of Conditional Discrimination and Inhibition: Implications for Psychiatric Disease
Sangha, S., & Fitzgerald, J. (2024) · Behavioral Neuroscience · doi:10.1037/bne0000594 · Cited by 2 · see citing works
“Falls and Davis (1995) have previously investigated the role of the central amygdala in conditioned inhibition of an FPS response by lesioning the CeA after training to a safety cue in rats.”
microRNA expression in learned safety
Ronovsky, M. (2013) · doi:10.25006/ia.1.s1-a1.24

Authors: Falls, W. A., & Davis, M.
Affiliations: Yale University (US)
Venue: Behavioral Neuroscience
Publisher: American Psychological Association (APA)
Published: 1995-06
Volume: 109
Issue: 3
Pages: 379-387
ISSN: 0735-7044 (ISSN-L)
1939-0084
DOI: 10.1037/0735-7044.109.3.379
OpenAlex: W4242505194
Cited by: 110
References: 0
Citations by year: 2025: 1 · 2024: 2 · 2023: 5 · 2021: 2 · 2020: 3 · 2018: 3 · 2017: 4 · 2016: 2 · 2015: 1 · 2014: 1 · 2013: 4 · 2012: 3
FWCI: 2.98
Type: journal article
Language: en
Open access: closed
Locations: Behavioral Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH 25642, MH 47840, MH 00004, P01MH025642)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: central amygdala, fear conditioning, conditioned inhibition, fear potentiation, fear-potentiated startle, lesion studies, startle response
MeSH terms: Amygdala, Animals, Arousal, Association Learning, Brain Mapping, Conditioning, Classical, Dominance, Cerebral, Electroshock, Fear, Male, Neural Inhibition, Photic Stimulation, Reflex, Startle, Rats, Sprague-Dawley, Rats

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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.

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