Onset and offset of aversive events establish distinct memories requiring fear and reward networks
- Marta Andreatta1,6,
- Markus Fendt2,6,7,
- Andreas Mühlberger1,
- Matthias J. Wieser1,
- Stefan Imobersteg2,
- Ayse Yarali3,
- Bertram Gerber4,5 and
- Paul Pauli1,7
- 1Department of Psychology, Julius Maximilians University, 97070 Würzburg, Germany
- 2Neuropsychiatry, Novartis Institutes for BioMedical Research, 4056 Basel, Switzerland
- 3Max Planck Institute of Neurobiology, 82152 Martinsried, Germany
- 4Leibniz Institute of Neurobiology (LIN), Department of Genetics of Learning and Memory, 39104 Magdeburg, Germany
- 5Institute of Biology, Department of Behavioural Genetics, Otto von Guericke University, 39104 Magdeburg, Germany
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↵6 These authors contributed equally to this work.
Abstract
Two things are worth remembering about an aversive event: What made it happen? What made it cease? If a stimulus precedes an aversive event, it becomes a signal for threat and will later elicit behavior indicating conditioned fear. However, if the stimulus is presented upon cessation of the aversive event, it elicits behavior indicating conditioned “relief.” What are the neuronal bases for such learning? Using functional magnetic resonance imaging (fMRI) in humans we found that a fear-conditioned stimulus activates amygdala but not striatum, whereas a relief-conditioned stimulus activates striatum but not amygdala. Correspondingly, acute inactivation of amygdala or of ventral striatum in rats respectively abolished only conditioned fear or only conditioned relief. Thus, the behaviorally opponent memories supported by onset and offset of aversive events engage and require fear and reward networks, respectively. This may explain attraction to stimuli associated with the cessation of trauma or of panic attacks.
Footnotes
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↵7 Corresponding authors
E-mail markus.fendt{at}web.de
E-mail pauli{at}mail.uni-wuerzburg.de
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[Supplemental material is available for this article.]
- Received May 2, 2012.
- Accepted July 29, 2012.
- © 2012 Cold Spring Harbor Laboratory Press
Freely available online through the Learning & Memory Open Access option.
