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The Journal of Neuroscience, August 4, 2004, 24(31):6912-6919; doi:10.1523/JNEUROSCI.1828-04.2004

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Behavioral/Systems/Cognitive
Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning

Gavan P. McNally, Michael Pigg, and Gabrielle Weidemann

School of Psychology, The University of New South Wales, Sydney, New South Wales 2052, Australia

Four experiments studied the role of opioid receptors in the midbrain periaqueductal gray matter (PAG), an important structure eliciting conditioned fear responses, in the extinction of Pavlovian fear. Rats received pairings of an auditory conditioned stimulus (CS) with a foot shock unconditioned stimulus (US). The freezing conditioned response (CR) elicited by the CS was then extinguished via nonreinforced presentations of the CS. Microinjection of the opioid receptor antagonist naloxone into the ventrolateral PAG (vlPAG) before nonrein-forced CS presentations impaired development of extinction, but such microinjections at the end of extinction did not reinstate an already extinguished freezing CR. This role for opioid receptors in fear extinction was specific to the vlPAG because infusions of naloxone into the dorsal PAG did not impair fear extinction. Finally, the impairment of fear extinction produced by vlPAG infusions of naloxone was dose-dependent. These results show for the first time that the midbrain PAG contributes to fear extinction and specifically identify a role for vlPAG opioid receptors in the acquisition but not the expression of such extinction. Taken together with our previous findings, we suggest that, during fear conditioning, activation of vlPAG opioid receptors contributes to detection of the discrepancy between the actual and expected outcome of the conditioning trial. vlPAG opioid receptors regulate the learning that accrues to the CS and other stimuli present on a trial because they instantiate an associative error correction process influencing US information reaching the site of CS-US convergence in the amygdala. During nonreinforcement, this vlPAG opioid receptor contribution signals extinction.

Key words: learning; memory; extinction; fear conditioning; periaqueductal gray; opioid receptor

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Received March 16, 2004; revised June 6, 2004; accepted June 7, 2004.

This article has been cited by other articles:

				F. Eippert, U. Bingel, E. Schoell, J. Yacubian, and C. Buchel Blockade of Endogenous Opioid Neurotransmission Enhances Acquisition of Conditioned Fear in Humans J. Neurosci., May 21, 2008; 28(21): 5465 - 5472. [Abstract] [Full Text] [PDF]

				J. M. Langton, J. H. Kim, J. Nicholas, and R. Richardson The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat Learn. Mem., September 25, 2007; 14(10): 665 - 668. [Abstract] [Full Text] [PDF]

				S. Cole and G. P. McNally Opioid receptors mediate direct predictive fear learning: Evidence from one-trial blocking Learn. Mem., April 2, 2007; 14(4): 229 - 235. [Abstract] [Full Text] [PDF]

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