A Developmental Neurobiological Model of Motivated Behavior: Anatomy, Connectivity and Ontogeny of the Triadic Nodes

Mood and Anxiety Disorders, Program National Institute of Mental Health, National Institutes of Health, 15K North Drive, Bethesda, MD 20892, United States
Neuroscience & Biobehavioral Reviews (Impact Factor: 8.8). 03/2009; 33(3):367-382. DOI: 10.1016/j.neubiorev.2008.10.009


Adolescence is the transition period that prepares individuals for fulfilling their role as adults. Most conspicuous in this transition period is the peak level of risk-taking behaviors that characterize adolescent motivated behavior. Significant neural remodeling contributes to this change. This review focuses on the functional neuroanatomy underlying motivated behavior, and how ontogenic changes can explain the typical behavioral patterns in adolescence. To help model these changes and provide testable hypotheses, a neural systems-based theory is presented. In short, the Triadic Model proposes that motivated behavior is governed by a carefully orchestrated articulation among three systems, approach, avoidance and regulatory. These three systems map to distinct, but overlapping, neural circuits, whose representatives are the striatum, the amygdala and the medial prefrontal cortex. Each of these system-representatives will be described from a functional anatomy perspective that includes a review of their connectivity and what is known of their ontogenic changes.

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    • "The vulnerability of adolescents to excessive alcohol use is thought to be promoted by an immature balance between cortical and limbic brain systems, including cortical control over dopaminergic pathways (Crews et al. 2007; Ernst and Fudge 2009; Chartier et al. 2010). Many aspects of dopamine transmission are dynamic during adolescence; for example, the density of dopamine receptors typically increases (Andersen et al. 2000; McCutcheon and Marinelli 2009; Jucaite et al. 2010) and spontaneous firing rates of dopamine neurons are higher (McCutcheon et al. 2012). "
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    ABSTRACT: Rationale Early onset of alcohol drinking has been associated with alcohol abuse in adulthood. The neurobiology of this phenomenon is unclear, but mesolimbic dopamine pathways, which are dynamic during adolescence, may play a role. Objectives We investigated the impact of adolescent binge-like alcohol on phasic dopaminergic neurotransmission during adulthood. Methods Rats received intermittent intragastric ethanol, water, or nothing during adolescence. In adulthood, electrically evoked dopamine release and subsequent uptake were measured in the nucleus accumbens core at baseline and after acute challenge of ethanol or saline. Results Adolescent ethanol exposure did not alter basal measures of evoked dopamine release or uptake. Ethanol challenge dose-dependently decreased the amplitude of evoked dopamine release in rats by 30–50 % in control groups, as previously reported, but did not alter evoked release in ethanol-exposed animals. To address the mechanism by which ethanol altered dopamine signaling, the evoked signals were modeled to estimate dopamine efflux per impulse and the velocity of the dopamine transporter. Dopamine uptake was slower in all exposure groups after ethanol challenge compared to saline, while dopamine efflux per pulse of electrical stimulation was reduced by ethanol only in ethanol-naive rats. Conclusions The results demonstrate that exposure to binge levels of ethanol during adolescence blunts the effect of ethanol challenge to reduce the amplitude of phasic dopamine release in adulthood. Large dopamine transients may result in more extracellular dopamine after alcohol challenge in adolescent-exposed rats and may be one mechanism by which alcohol is more reinforcing in people who initiated drinking at an early age.
    No preview · Article · Oct 2015 · Psychopharmacology
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    • "The interaction of emotion and executive control of behavior is a crucial focal point for understanding the neural basis of decision making in high-risk situations such as those involving drug use or self-harm. Explanations of high risk behavior tendencies have emphasized individual differences and developmental changes in emotion processes, reward processing, and executive control of behavior and emotions (Jessor, 1991; Arnett, 1992, 1994, 1996; Ernst et al., 2006; Steinberg, 2007; Casey et al., 2008; Ernst and Mueller, 2008; Gullo and Dawe, 2008; Steinberg, 2008; Ernst and Fudge, 2009; Romer et al., 2009; Romer, 2010; Casey et al., 2011; Dalley et al., 2011; Mitchell, 2011; Blakemore and Robbins, 2012; Whelan et al., 2012). We used an emotional Go/NoGo task with functional magnetic resonance imaging (fMRI) to investigate processes related to response inhibition and emotion processing in a sample of 21 adolescents (age 14–17 years) with a range of risk behavior tendencies. "
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    ABSTRACT: High-risk behavior in adolescents is associated with injury, mental health problems, and poor outcomes in later life. Improved understanding of the neurobiology of high-risk behavior and impulsivity shows promise for informing clinical treatment and prevention as well as policy to better address high-risk behavior. We recruited 21 adolescents (age 14–17) with a wide range of high-risk behavior tendencies, including medically high-risk participants recruited from psychiatric clinics. Risk tendencies were assessed using the Adolescent Risk Behavior Screen (ARBS). ARBS risk scores correlated highly (0.78) with impulsivity scores from the Barratt Impulsivity scale (BIS). Participants underwent 4.7 Tesla functional magnetic resonance imaging (fMRI) while performing an emotional Go/NoGo task. This task presented an aversive or neutral distractor image simultaneously with each Go or NoGo stimulus. Risk behavior and impulsivity tendencies exhibited similar but not identical associations with fMRI activation patterns in prefrontal brain regions. We interpret these results as reflecting differences in response inhibition, emotional stimulus processing, and emotion regulation in relation to participant risk behavior tendencies and impulsivity levels. The results are consistent with high impulsivity playing an important role in determining high risk tendencies in this sample containing clinically high-risk adolescents.
    Full-text · Article · Sep 2015 · Frontiers in Systems Neuroscience
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    • "Furthermore, EC has been associated with the function of the executive attention network during cognitive tasks such as task switching, working memory tasks and sequential inhibition tasks (Posner and Rothbart, 2009; Posner, 2012). These tasks have been related to activity in the frontoparietal attention system (Ernst and Fudge, 2009). For example, functional neuroimaging studies suggest that dispositional EC is positively associated with activities in the prefrontal cortex (PFC) and posterior parietal regions (Kanske and Kotz, 2013; Kennis et al., 2013). "
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    ABSTRACT: Structural MRI studies have identified a link between cortical maturation and temperamental effortful control (EC), which is a trait-like risk factor for psychopathology during adolescence. However, little research has explored the underlying neural basis of EC in adults. We aimed to examine the relationship between EC and brain structure in young adults. High-resolution T1-weighted images were acquired from 27 undergraduates who completed the Adult Temperament Questionnaire-short form. The data were analyzed with SPM8 using voxel-based morphometry (VBM). A priori region of interest (ROI) analyses indicated that EC was positively associated with gray matter volumes in brain regions that included the bilateral dorsolateral prefrontal cortex, the left supplementary motor area, the right orbitofrontal cortex, the left anterior cingulate cortex, and the left superior and inferior parietal lobes. These results suggest that temperamental EC in young adults is related to variations in gray matter volumes, particularly within the frontoparietal attention network, and yield insight into the relation between the vulnerability to psychopathology and the neurobiological basis of individual differences in temperamental EC. Copyright © 2015 Elsevier Ireland Ltd. All rights reserved.
    Full-text · Article · May 2015 · Psychiatry Research: Neuroimaging
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