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The Journal of Neuroscience, December 26, 2007, 27(52):14358-14364; doi:10.1523/JNEUROSCI.4508-07.2007

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Behavioral/Systems/Cognitive
Dimensions of Impulsivity Are Associated with Poor Spatial Working Memory Performance in Monkeys

Alex S. James,^1 * Stephanie M. Groman,^1 * Emanuele Seu,¹ Matthew Jorgensen,² Lynn A. Fairbanks,² and J. David Jentsch^1,2

Departments of ¹Psychology and ²Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, California 90095

Correspondence should be addressed to Dr. J. David Jentsch, Department of Psychology, University of California, Los Angeles, P.O. Box 951563, Los Angeles, CA 90095-1563. Email: jentsch{at}psych.ucla.edu

Impulsive behavior and novelty seeking are dimensions of temperament that are behavioral determinants of risk for attention deficit/hyperactivity disorder and its neurocognitive endophenotypes, and variation in the dopamine D₄ receptor gene (DRD4) explains at least a portion of the variance in the traits. To further characterize the dimensional phenotype associated with impulsiveness, adolescent male monkeys were evaluated using ecologically valid tests of impulsive approach and aggression in response to social or nonsocial stimuli; subsequently, a delayed response task was implemented to assess spatial working memory performance. Subjects were selected into this study based on their response to the social challenge task or by DRD4 genotype, resulting in three groups: low-impulsivity/common DRD4 allele, high-impulsivity/common DRD4 allele, or rare DRD4 allele. All animals acquired the delayed response task and could perform at near ceiling levels when a 0 s delay version was imposed, but as delays were lengthened, high-impulsive animals, regardless of DRD4 genotype, made fewer correct responses than did low-impulsive subjects; an inverse relationship existed for working memory and impulsivity. Notably, impulsive behavior evoked by social and nonsocial stimuli explained overlapping and independent portions of the variance in working memory performance. CSF levels of monoamine metabolites did not significantly differentiate the high- and low-impulsive animals, although monkeys carrying the DRD4 rare allele tended to exhibit higher monoamine turnover. These data indicate that dimensions of impulsivity may impact on working memory performance in qualitatively similar ways but through different mechanisms.

Key words: dopamine; ADHD; cognition; temperament; serotonin; prefrontal cortex

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Received July 30, 2007; revised Nov. 14, 2007; accepted Nov. 14, 2007.

Correspondence should be addressed to Dr. J. David Jentsch, Department of Psychology, University of California, Los Angeles, P.O. Box 951563, Los Angeles, CA 90095-1563. Email: jentsch{at}psych.ucla.edu

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