Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice

Lewis, Michael C.; Gould, Thomas J.

doi:10.1002/hipo.20284

Cited by 42Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMemory Processes and Influences

Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice

Lewis, Michael C., Gould, Thomas J.·2007·Hippocampus

DOI 10.1002/hipo.20284

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Abstract

For latent inhibition, preexposure to a conditioned stimulus (CS) prior to training with an unconditioned stimulus (US) results in decreased conditioned responses (CRs) to the CS at the time of testing. The mechanism by which decreased CRs occurs, however, is unknown; CS preexposure may interfere with subsequent conditioning, or modulate the expression of CRs. Previous research has suggested that the entorhinal cortex (EC) is necessary for latent inhibition of a variety of tasks. However, no studies have specifically compared the role of the EC in acquisition vs. expression of latent inhibition. The present study used reversible inactivation of the EC to address this issue. The GABA agonist muscimol (0.5 μg/side) was directly infused into the EC of mice prior to CS preexposure, training, or testing. Our results indicate that muscimol inactivation of the EC before CS preexposure disrupts latent inhibition of cued fear conditioning. Importantly, this same dose of muscimol did not disrupt cued fear conditioning, nor did it affect latent inhibition when infused into the subiculum. Furthermore, inactivation of the EC at testing disrupted the expression of latent inhibition of cued fear conditioning; that is, CS preexposed mice that received entorhinal cortical muscimol infusion at testing showed CRs compared to saline‐infused CS preexposed mice. These findings suggest that repeated preexposure to the CS during latent inhibition may alter entorhinal cortical activity thereby allowing the EC to exert inhibitory control over the expression of CRs during testing of CS preexposed mice. © 2007 Wiley‐Liss, Inc.

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Direct infusions into the ventral hippocampus have very good anatomical precision, with spread of infusion using this procedure about 1 mm3 after 24-48 h.
“Direct infusions, as opposed to i.c.v. or systemic infusions, have very good anatomical precision, as the spread of infusion using this procedure is B1 mm3 after 24–48 h (Davis et al, 2007; Lewis and Gould, 2007).”
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The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258 · see citing works
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896 · see citing works
The Emotional Brain, Fear, and the Amygdala
LeDoux, J. (2003) · Cellular and Molecular Neurobiology · doi:10.1023/a:1025048802629 · Cited by 1,818 · see citing works
Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear
LeDoux, J., Iwata, J., Cicchetti, P., & Reis, D. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02517.1988 · Cited by 1,580 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Latent inhibition and conditioned attention theory.
Lubow, R. E., Schnur, P., & Rifkin, B. (1976) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.2.2.163 · Cited by 733 · see citing works
Latent Inhibition and Conditioned Attention Theory
Lubow, R. E. (1989) · Cambridge University Press eBooks · doi:10.1017/cbo9780511529849 · Cited by 697 · see citing works
The Neuroscience of Mammalian Associative Learning
Fanselow, M. S., & Poulos, A. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070213 · Cited by 683 · see citing works
The Parahippocampal Region: Corticocortical Connectivity
Burwell, R. D. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06717.x · Cited by 513 · see citing works
Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat
Martin, J. H. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90784-q · Cited by 459 · see citing works
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · cited 1× · see citing works
“This dose of muscimol has also been shown to disrupt the context-specific expression of both latent inhibition of cued fear conditioning and extinction of cued fear conditioning (Holt and Maren, 1999; Corcoran and Maren, 2001).”
The "two-headed" latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment
Weiner, I. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1313-x · Cited by 387 · see citing works
An Inhibitory Interface Gates Impulse Traffic between the Input and Output Stations of the Amygdala
Royer, S., Martina, M., & Paré, D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10575.1999 · Cited by 350 · see citing works
Context specificity of conditioning, extinction, and latent inhibition.
Lovibond, P. F., Preston, G. C., & Mackintosh, N. J. (1984) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.10.3.360 · Cited by 218 · see citing works
Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory
Holt, W., & Maren, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09054.1999 · Cited by 213 · see citing works
Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses
Royer, S., & Paré, D. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00455-4 · Cited by 210 · see citing works
The intercalated cell masses project to the central and medial nuclei of the amygdala in cats
Paré, D., & Smith, Y. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90050-p · Cited by 209 · see citing works
Differential effects of contextual change on latent inhibition and on the habituation of an orienting response.
Hall, G., & Channell, S. (1985) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.11.3.470 · Cited by 181 · see citing works
Muscimol Diffusion after Intracerebral Microinjections: A Reevaluation Based on Electrophysiological and Autoradiographic Quantifications
Edeline, J., Hars, B., Hennevin, E., & Cotillon, N. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4035 · Cited by 157 · see citing works
Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats.
Maren, S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.2.283 · Cited by 153 · see citing works
Distribution of GABA immunoreactivity in the amygdaloid complex of the cat
Paré, D., & Smith, Y. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90049-l · Cited by 152 · see citing works
Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat.
McDonald, A., & Mascagni, F. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00478-2 · Cited by 142 · see citing works
Contextual effects in latent inhibition with an appetitive conditioning procedure
Channell, S., & Hall, G. (1983) · Animal Learning & Behavior · doi:10.3758/bf03212309 · Cited by 134 · see citing works
Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats.
Maren, S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.2.283 · Cited by 127 · see citing works
A Search for Context-Stimulus Associations in Latent Inhibition
Hall, G., & Minor, H. (1984) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/14640748408402200 · Cited by 125 · see citing works
Entorhinal but Not Hippocampal or Subicular Lesions Disrupt Latent Inhibition in Rats
Coutureau, É., Galani, R., Gosselin, O., Majchrzak, M. J., & Scala, G. D. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3895 · Cited by 94 · see citing works
Historical context of state dependent learning and discriminative drug effects
Overton, D. A. (1991) · Behavioural Pharmacology · doi:10.1097/00008877-199109000-00002 · Cited by 88 · see citing works
Dissociating entorhinal and hippocampal involvement in latent inhibition.
Daphna Shohamy, A., Allen, M. T., & Gluck, M. A. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.5.867 · Cited by 63 · see citing works
Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions?
Sewards, T. V., & Sewards, M. A. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(03)00175-9 · Cited by 59 · see citing works
Attenuation of Latent Inhibition by Post-Acquisition Reminder
Kasprow, W. J., Catterson, D. A., Schachtman, T. R., & Miller, R. R. (1984) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/14640748408402194 · Cited by 58 · see citing works
The influence of selective lesions to components of the hippocampal system on the orientating response, habituation and latent inhibition
Oswald, C. J. P., Yee, B. K., Rawlins, J. N. P., Bannerman, D. M., Good, M. A., & Honey, R. C. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02028.x · Cited by 55 · see citing works
Nicotine enhances latent inhibition and ameliorates ethanol-induced deficits in latent inhibition
Gould, T. J., Collins, A. C., & Wehner, J. M. (2001) · Nicotine & Tobacco Research · doi:10.1080/14622200020032060 · Cited by 53 · see citing works
Self-citation
Postconditioning recovery from the latent inhibition effect in conditioned taste aversion
Bakner, L., Strohen, K., Marvin, N., et al. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90595-f · Cited by 47 · see citing works
Genetic influences on latent inhibition.
Gould, T. J., & Wehner, J. M. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1291 · Cited by 41 · see citing works
Self-citation
Contextual control of negative transfer produced by prior CS-US pairings
Swartzentruber, D., & Bouton, M. E. (1986) · Learning and Motivation · doi:10.1016/0023-9690(86)90004-4 · Cited by 37 · see citing works
Cytotoxic lesions of the retrohippocampal region attenuate latent inhibition but spare the partial reinforcement extinction effect
Yee, B. K., Feldon, J., & Rawlins, J. N. P. (1997) · Experimental Brain Research · doi:10.1007/pl00005694 · Cited by 35 · see citing works
The entorhinal cortex-nucleus accumbens pathway and latent inhibition: A behavioral and neurochemical study in rats.
Coutureau, É., Léna, I., Daugé, V., & Scala, G. D. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.1.95 · Cited by 26 · see citing works
The entorhinal cortex-nucleus accumbens pathway and latent inhibition: A behavioral and neurochemical study in rats.
Coutureau, É., Léna, I., Daugé, V., et al. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.1.95 · Cited by 25 · see citing works
Restoration of latent inhibition by olanzapine but not haloperidol in entorhinal cortex-lesioned rats
Coutureau, É., Gosselin, O., & Scala, G. D. (2000) · Psychopharmacology · doi:10.1007/s002130000434 · Cited by 23 · see citing works
Retention of latent inhibition in a taste-aversion paradigm
McIntosh, S. M., & Tarpy, R. M. (1977) · Bulletin of the Psychonomic Society · doi:10.3758/bf03337040 · Cited by 21 · see citing works
Latent inhibition of cued fear conditioning: an NMDA receptor‐dependent process that can be established in the presence of anisomycin
Lewis, M. C., & Gould, T. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03531.x · Cited by 20 · see citing works
Self-citation
Forgetting, preconditioning CS familiarization and taste aversion learning: An animal experiment with implications for alcoholism treatment
Elkins, R. L., & Hobbs, S. H. (1979) · Behaviour Research and Therapy · doi:10.1016/0005-7967(79)90100-1 · Cited by 18 · see citing works
Plasticity in the Entorhinal Cortex Suppresses Memory for Contextual Fear
Hebert, A. E., & Dash, P. K. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3491-04.2004 · Cited by 17 · see citing works
Striatal dopaminergic responses observed in latent inhibition are dependent on the hippocampal ventral subicular region
Peterschmitt, Y., Hoeltzel, A., & Louilot, A. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04366.x · Cited by 13 · see citing works
Latent inhibition from context-dependent retrieval of conflicting information
Wright, D. C., Skala, K. D., & Peuser, K. A. (1986) · Bulletin of the Psychonomic Society · doi:10.3758/bf03330531 · Cited by 12 · see citing works

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Authors: Lewis, M. C., & Gould, T. J.
Affiliations: Temple University (US)
Corresponding author: Gould, Thomas J.
ORCID: Gould, Thomas J.
Venue: Hippocampus
Publisher: Wiley
Published: 2007-03-19
Volume: 17
Issue: 6
Pages: 462-470
ISSN: 1050-9631 (ISSN-L)
1098-1063
DOI: 10.1002/hipo.20284
OpenAlex: W2123774285
Cited by: 42
References: 46
Citations by year: 2026: 1 · 2022: 3 · 2019: 1 · 2018: 2 · 2017: 1 · 2014: 2 · 2013: 6 · 2012: 3
FWCI: 3.34
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Hippocampus (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Drug Abuse (DA017949, R01DA017949)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: entorhinal cortex, latent inhibition, cued fear conditioning, muscimol inactivation, subiculum, inhibitory control, hippocampal formation
MeSH terms: Analysis of Variance, Animals, Behavior, Animal, Conditioning, Classical, Cues, Fear, Inhibition, Psychological, Male, Mice, Inbred C57BL, Muscimol, Time Factors, Entorhinal Cortex, GABA Agonists, Mice

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Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice

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