Drug abuse and addiction are severe disorders characterized by excessive and compulsive drug consumption, affecting millions of individuals in the Western world. Converging evidence shows that long-term exposure to drugs affects subcortically mediated hedonic and emotional learning processes, as well as cortically dependent decisions. An important source of decision bias in drug abuse comes from Pavlovian stimuli and contexts which, by virtue of their association with drugs of abuse gain incentive salience and the power to influence actions. In addicted individuals, the mere exposure to drug-associated cues can motivate further drug consumption or even trigger relapse after a period of abstinence. Despite the importance of these Pavlovian effects on cognitive decisions, their neural mechanisms remain unknown. Recently we discovered that Pavlovian learning strongly affects activity related to attention and eye movements in a cortical association area, the lateral intraparietal area (LIP) of the monkey. Conditioned stimuli predicting reward (""""""""good news"""""""") attract attention and produce local excitation in the spatial attention map in LIP;stimuli conditioned to predict no reward (""""""""bad news"""""""") repel attention from their location and produce local inhibition in LIP. Like the effects described in rodents and humans, the effects in our study arose automatically and persisted even though they interfered with performance;moreover, after prolonged training the effects increased and became habitual, partly resistant to contextual control.
We aim to extend these findings by testing whether, in addition to biasing simple orienting, Pavlovian stimuli also bias more complex decisions that are not spatially related to the cues. These studies are innovative because they establish a new link between two disparate research traditions - the study of Pavlovian learning (traditionally conducted in rodents using pharmacological and behavioral methods) and the study of decision formation (traditionally conduced in monkeys using single-neuron recordings). Thus, they will provide insight into interactions between emotional learning and decision formation in normal behavior and in relation to drug abuse, and may suggest cognitive strategies for overcoming the power of emotional learning when this learning has undesirable, maladaptive effects. 1

Public Health Relevance

Abundant evidence shows that Pavlovian learning plays an important role in drug abuse. Cues or environments associated with drugs of abuse gain incentive salience and the power to elicit cravings, potentially contributing to the maintenance or relapse of drug consumption. To understand the mechanisms of these effects we test the influence of Pavlovian learning on attention using single-neuron recording in a parietal area related to attention and decision formation in rhesus monkeys. The long-term goal is to understand interactions between emotional learning and cognitive decisions in normal behavior and drug addiction. 1

National Institute of Health (NIH)
National Institute on Drug Abuse (NIDA)
Exploratory/Developmental Grants (R21)
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Special Emphasis Panel (ZDA1-GXM-A (13))
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Volman, Susan
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Columbia University (N.Y.)
Schools of Medicine
New York
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Gottlieb, Jacqueline; Oudeyer, Pierre-Yves; Lopes, Manuel et al. (2013) Information-seeking, curiosity, and attention: computational and neural mechanisms. Trends Cogn Sci 17:585-93
Suzuki, Mototaka; Gottlieb, Jacqueline (2013) Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe. Nat Neurosci 16:98-104