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The Journal of Neuroscience, April 12, 2006, 26(15):4036-4045; doi:10.1523/JNEUROSCI.4679-05.2006

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Behavioral/Systems/Cognitive
Opioid Receptors in the Nucleus Accumbens Regulate Attentional Learning in the Blocking Paradigm

Mihaela D. Iordanova, Gavan P. McNally, and R. Frederick Westbrook

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

Correspondence should be addressed to Dr. R. Frederick Westbrook, School of Psychology, The University of New South Wales, Sydney, New South Wales 2052, Australia. Email: f.westbrook{at}unsw.edu.au

Fear learning depends on prediction error, or the discrepancy between the actual and expected outcome of a conditioning trial. These experiments used blocking and unblocking designs to study the role of opioid receptors in the nucleus accumbens (Acb) in predictive fear learning. Previous fear conditioning to a context blocked later fear conditioning to a conditioned stimulus (CS) in that context. Fear learning proceeded normally (i.e., unblocking occurred) if the CS signaled a more intense footshock than was used during previous context conditioning. Blocking and unblocking were mediated by Acb opioid receptors. Acb microinjections of a nonselective opioid receptor agonist prevented blocking, whereas a nonselective antagonist prevented unblocking. Examination of the associative mechanism for blocking and unblocking revealed that Acb opioid receptors mediate indirect predictive learning by controlling learned variations in attention. µ-Opioid and -opioid receptors contribute to this learned regulation of attention because Acb microinjections of a µ-opioid receptor agonist impaired, whereas a -opioid receptor agonist facilitated, blocking. Acb microinjections of a µ-opioid receptor antagonist also prevented unblocking. Microinjections of a -opioid receptor agonist or antagonist were without effect on blocking and unblocking. Our data show that the Acb mediates attentional selection between competing predictors of motivationally significant events to enable learning about the best predictor of such events at the expense of worse predictors. During fear learning, Acb µ-opioid receptors upregulate attention to conditioned stimuli that are predictive of shock, whereas -opioid receptors downregulate attention to conditioned stimuli that are redundant or noninformative predictors of shock.

Key words: learning; blocking; unblocking; attention; opioid receptor; prediction error

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Received Nov. 1, 2005; revised Feb. 23, 2006; accepted Feb. 25, 2006.

Correspondence should be addressed to Dr. R. Frederick Westbrook, School of Psychology, The University of New South Wales, Sydney, New South Wales 2052, Australia. Email: f.westbrook{at}unsw.edu.au

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]

				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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