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The Journal of Neuroscience, December 27, 2006, 26(52):13556-13566; doi:10.1523/JNEUROSCI.3713-06.2006

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Behavioral/Systems/Cognitive
Extracellular Hippocampal Acetylcholine Level Controls Amygdala Function and Promotes Adaptive Conditioned Emotional Response

Ludovic Calandreau,¹ Pierre Trifilieff,¹ Nicole Mons,¹ Laurence Costes,^1,2 Marc Marien,³ Aline Marighetto,¹ Jacques Micheau,¹ Robert Jaffard,¹ and Aline Desmedt¹

¹Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5106, Laboratoire de Neurosciences Cognitives, 33405 Talence, France, ²Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1244, Institut François Magendie, 33077 Bordeaux cedex, France, and ³Centre de Recherche Pierre Fabre, Division de Neurobiologie I, 81106 Castres, France

Correspondence should be addressed to Dr. Aline Desmedt, Laboratoire de Neurosciences Cognitives, Avenue des Facultés, 33405 Talence, France. Email: a.desmedt{at}lnc.u-bordeaux1.fr

Ample data indicate that tone and contextual fear conditioning differentially require the amygdala and the hippocampus. However, mechanisms subserving the adaptive selection among environmental stimuli (discrete tone vs context) of those that best predict an aversive event are still elusive. Because the hippocampal cholinergic neurotransmission is thought to play a critical role in the coordination between different memory systems leading to the selection of appropriate behavioral strategies, we hypothesized that this cholinergic signal may control the competing acquisition of amygdala-mediated tone and contextual conditioning. Using pavlovian fear conditioning in mice, we first show a higher level of hippocampal acetylcholine release and a specific pattern of extracellular signal-regulated kinase 1/2 (ERK1/2) activation within the lateral (LA) and basolateral (BLA) amygdala under conditions in which the context is a better predictor than a discrete tone stimulus. Second, we demonstrate that levels of hippocampal cholinergic neurotransmission are causally related to the patterns of ERK1/2 activation in amygdala nuclei and actually determine the selection among the context or the simple tone the stimulus that best predicts the aversive event. Specifically, decreasing the hippocampal cholinergic signal not only impaired contextual conditioning but also mimicked conditioning to the discrete tone, both in terms of the behavioral outcome and the LA/BLA ERK1/2 activation pattern. Conversely, increasing this cholinergic signal not only disrupted tone conditioning but also promoted contextual fear conditioning. Hence, these findings highlight that hippocampal cholinergic neurotransmission controls amygdala function, thereby leading to the selection of relevant emotional information.

Key words: acetylcholine; amygdala; ERK; fear; hippocampus; pavlovian conditioning

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Received Feb. 6, 2006; revised Nov. 27, 2006; accepted Nov. 28, 2006.

Correspondence should be addressed to Dr. Aline Desmedt, Laboratoire de Neurosciences Cognitives, Avenue des Facultés, 33405 Talence, France. Email: a.desmedt{at}lnc.u-bordeaux1.fr

This article has been cited by other articles:

				R. P. Alvarez, A. Biggs, G. Chen, D. S. Pine, and C. Grillon Contextual Fear Conditioning in Humans: Cortical-Hippocampal and Amygdala Contributions J. Neurosci., June 11, 2008; 28(24): 6211 - 6219. [Abstract] [Full Text] [PDF]

				L. G. Reijmers, B. L. Perkins, N. Matsuo, and M. Mayford Localization of a Stable Neural Correlate of Associative Memory Science, August 31, 2007; 317(5842): 1230 - 1233. [Abstract] [Full Text] [PDF]

				L. Calandreau, R. Jaffard, and A. Desmedt Dissociated roles for the lateral and medial septum in elemental and contextual fear conditioning Learn. Mem., June 6, 2007; 14(6): 422 - 429. [Abstract] [Full Text] [PDF]

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