Calculating Consequences: Brain Systems That Encode the Causal Effects of Actions

Division of the Humanities and Social Sciences and Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 07/2008; 28(26):6750-5. DOI: 10.1523/JNEUROSCI.1808-08.2008
Source: PubMed

ABSTRACT The capacity to accurately evaluate the causal effectiveness of our actions is key to successfully adapting to changing environments. Here we scanned subjects using functional magnetic resonance imaging while they pressed a button to earn money as the response-reward relationship changed over time. Subjects' judgments about the causal efficacy of their actions reflected the objective contingency between the rate of button pressing and the amount of money they earned. Neural responses in medial orbitofrontal cortex and dorsomedial striatum were modulated as a function of contingency, by increasing in activity during sessions when actions were highly causal compared with when they were not. Moreover, medial prefrontal cortex tracked local changes in action-outcome correlations, implicating this region in the on-line computation of contingency. These results reveal the involvement of distinct brain regions in the computational processes that establish the causal efficacy of actions, providing insight into the neural mechanisms underlying the adaptive control of behavior.

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Available from: Bernard W Balleine, Sep 29, 2015
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    • "Yet, much of the animal literature relies on devaluation paradigms that utilize immediate outcomes (Balleine and O'Doherty, 2010). Similarly, experiments in humans have implicated anterior caudate in outcome devaluation (Valentin et al., 2007) and in tracking contingencies between actions and outcomes (Tanaka et al., 2008), yet often do not require valuations that integrate immediate and longterm consequences. Thus, one possibility is that both vmPFC and anterior caudate support goals by representing outcomes (Valentin et al., 2007), while vmPFC predominantly receives the input required to calculate long-term value. "
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    ABSTRACT: The impulse to act for immediate reward often conflicts with more deliberate evaluations that support long-term benefit. The neural architecture that negotiates this conflict remains unclear. One account proposes a single neural circuit that evaluates both immediate and delayed outcomes, while another outlines separate impulsive and patient systems that compete for behavioral control. Here we designed a task in which a complex payout structure divorces the immediate value of acting from the overall long-term value, within the same outcome modality. Using model-based fMRI in humans, we demonstrate separate neural representations of immediate and long-term value, with the former tracked in anterior caudate (AC) and the latter in ventromedial prefrontal cortex (vmPFC). Crucially, when subjects' choices were compatible with long-run consequences, value signals in AC were down-weighted and those in vmPFC were enhanced, while the opposite occurred when choice was impulsive. Thus, our data implicate a trade-off in value representation between AC and vmPFC as underlying controlled versus impulsive choice. Copyright © 2014. Published by Elsevier Inc.
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    • "Although both action–outcome and stimulus–response learning appear to depend on the cortical-basal ganglia network the critical aspects of this network involved in the two forms of learning differ. Evidence from lesions (Yin et al., 2005), local inactivation (Yin et al., 2005) and various pharmacological manipulations (Yin et al., 2005; Shiflett et al., 2010) in rodents and neuroimaging studies in humans (Tanaka et al., 2008; b r a i n r e s e a r c h ] "
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    ABSTRACT: The recent focus of addiction research has been on effect of drug exposure on the neural processes that mediate the acquisition and performance of goal-directed instrumental actions. Deficits in goal-directed control and a consequent dysregulation of habit learning processes have been described as resulting in compulsive drug seeking. Similarly, considerable research has focussed on the motivational and emotional changes that drugs produce and that result in changes in the incentive processes that modulate goal-directed performance. Although these areas have developed independently, we argue that the effects they described are likely not independent. Here we hypothesize that these changes result from a core deficit in the way the learning and performance factors that support goal-directed action are integrated at a neural level to maintain behavioural control. A dorsal basal ganglia stream mediating goal-directed learning and a ventral stream mediating various performance factors find several points of integration in the cortical basal ganglia system, most notably in the thalamocortical network linking basal ganglia output to a variety of cortical control centres. Recent research in humans and other animals is reviewed suggesting that learning and performance factors are integrated in a network centred on the mediodorsal thalamus and that disintegration in this network may provide the basis for a 'switch' from recreational to dysregulated drug seeking resulting in the well documented changes associated with addiction. Copyright © 2014. Published by Elsevier B.V.
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    • "The pragmatic anticipation of the action's effects is mapped from PPC onto premotor and motor regions to activate the corresponding motor programs (Sirigu et al., 1996; Snyder et al., 2000). The neural activation patterns of pragmatic anticipation may in fact activate the descending motor pathways at subthreshold level (e.g., Jacobson, 1927; Tanaka et al., 2008). The pragmatic anticipation of an action's effects thus awakens, at least incipiently, the actual movement which is its object, often without one's awareness (Münsterberg , 1914). "
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    ABSTRACT: This paper presents a novel theoretical view on impulsive action, integrating thus far separate perspectives on non-reflective action, motivation, emotion regulation, and impulse control. We frame impulsive action in terms of directedness of the individual organism toward, away, or against other givens - toward future states and away from one's present state. First, appraisal of a perceived or thought-of event or object on occasion, rapidly and without premonition or conscious deliberation, triggers a motive to modify one's relation to that event or object. Situational specifics of the event as perceived and appraised motivate and guide selection of readiness for a particular kind of purposive action. Second, perception of complex situations can give rise to multiple appraisals, multiple motives, and multiple simultaneous changes in action readiness. Multiple states of action readiness may interact in generating action, by reinforcing or attenuating each other, thereby yielding impulse control. We show how emotion control can itself result from a motive state or state of action readiness. Our view links impulsive action mechanistically to states of action readiness, which is the central feature of what distinguishes one kind of emotion from another. It thus provides a novel theoretical perspective to the somewhat fragmented literature on impulsive action.
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