Contrasting Cortical and Subcortical Activations Produced by Attentional-Set Shifting and Reversal Learning in Humans

University of Cambridge and Medical Research Council, United Kingdom.
Journal of Cognitive Neuroscience (Impact Factor: 4.09). 01/2000; 12(1):142-62. DOI: 10.1162/089892900561931
Source: PubMed


Much evidence suggests that lesions of the prefrontal cortex (PFC) produce marked impairments in the ability of subjects to shift cognitive set, as exemplified by performance of the Wisconsin Card Sorting Test (WCST). However, studies with humans and experimental primates have suggested that damage to different regions of PFC induce dissociable impairments in two forms of shift learning implicit in the WCST (that is, extradimensional (ED) shift learning and reversal shift learning), with similar deficits also being apparent after damage to basal ganglia structures, especially the caudate nucleus. In this study, we used the same visual discrimination learning paradigm over multidimensional stimuli, and the H215O positron emission tomography (PET) technique, to examine regional cerebral blood flow (rCBF) changes associated with these subcomponent processes of the WCST. In three conditions, subjects were scanned while acquiring visual discriminations involving either (i) the same stimulus dimension as preceding discriminations (intradimensional (ID) shifts); (ii) different stimulus dimensions from previous discriminations (ED shifts) or (iii) reversed stimulus-reward contingencies (reversal shifts). Additionally, subjects were scanned while responding to already learnt discriminations ('performance baseline'). ED shift learning, relative to ID shift learning, produced activations in prefrontal regions, including left anterior PFC and right dorsolateral PFC (BA 10 and 9⁄46). By contrast, reversal learning, relative to ID shift learning, produced activations of the left caudate nucleus. Additionally, compared to reversal and ID shift learning, ED shift learning was associated with relative deactivations in occipito-temporal pathways (for example, BA 17 and 37). These results confirm that, in the context of visual discrimination learning over multidimensional stimuli, the control of an acquired attentional bias or'set', and the control of previously acquired stimulus-reinforcement associations, activate distinct cortical and subcortical neural stations. Moreover, we propose that the PFC may contribute to the control of attentional-set by modulating attentional processes mediated by occipito-temporal pathways.

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Available from: Thomasin C. Andrews, Aug 28, 2014
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    • "Lesion studies on animals [3], [13], [14], [15], [16] and humans [2], [17] have consistently implicated the ventrolateral prefrontal cortex and lateral orbitofrontal cortex (OFC) in this type of reversal learning. Mirroring these findings, functional imaging studies have also identified the lateral OFC [9], [18], [19], and several other brain regions in reversal learning, including the inferior frontal gyrus (IFG) [20], [21], the dorsomedial prefrontal cortex (DMPFC)[22], [23], the dorsolateral prefrontal cortex (DLPFC) [23], [24], the posterior parietal cortex [25], [26], and the striatum [20], [27], [28], [29], [30], [31]. "
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    ABSTRACT: Impairments in flexible goal-directed decisions, often examined by reversal learning, are associated with behavioral abnormalities characterized by impulsiveness and disinhibition. Although the lateral orbital frontal cortex (OFC) has been consistently implicated in reversal learning, it is still unclear whether this region is involved in negative feedback processing, behavioral control, or both, and whether reward and punishment might have different effects on lateral OFC involvement. Using a relatively large sample (N = 47), and a categorical learning task with either monetary reward or moderate electric shock as feedback, we found overlapping activations in the right lateral OFC (and adjacent insula) for reward and punishment reversal learning when comparing correct reversal trials with correct acquisition trials, whereas we found overlapping activations in the right dorsolateral prefrontal cortex (DLPFC) when negative feedback signaled contingency change. The right lateral OFC and DLPFC also showed greater sensitivity to punishment than did their left homologues, indicating an asymmetry in how punishment is processed. We propose that the right lateral OFC and anterior insula are important for transforming affective feedback to behavioral adjustment, whereas the right DLPFC is involved in higher level attention control. These results provide insight into the neural mechanisms of reversal learning and behavioral flexibility, which can be leveraged to understand risky behaviors among vulnerable populations.
    PLoS ONE 12/2013; 8(12):e82169. DOI:10.1371/journal.pone.0082169 · 3.23 Impact Factor
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    • "The attentional set-shifting task has been developed as a non-human primate version of the WCST (Roberts et al., 1988). Because it is a more direct measure of the ability to shift cognitive set and a better measure for frontal lobe impairments (Rogers et al., 2000), it is now often used in human subjects as well. Both reversal learning and attentional set-shifting paradigms have been developed for humans, non-human primates and rodents. "
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    ABSTRACT: Striatal dopamine (DA) is thought to code for learned associations between cues and reinforcers and to mediate approach behavior toward a reward. Less is known about the contribution of DA to cognitive flexibility-the ability to adapt behavior in response to changes in the environment. Altered reward processing and impairments in cognitive flexibility are observed in psychiatric disorders such as obsessive compulsive disorder (OCD). Patients with this disorder show a disruption of functioning in the frontostriatal circuit and alterations in DA signaling. In this review we summarize findings from animal and human studies that have investigated the involvement of striatal DA in cognitive flexibility. These findings may provide a better understanding of the role of dopaminergic dysfunction in cognitive inflexibility in psychiatric disorders, such as OCD.
    Frontiers in Neuroscience 11/2013; 7(7):201. DOI:10.3389/fnins.2013.00201 · 3.66 Impact Factor
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    • "Similarly, lesion studies of non-human primates in a similar paradigm are commensurate with these findings (e.g., Dias, Robbins, & Roberts, 1996; Dias, Robbins, & Roberts, 1997). Rogers et al. (2000) also reported similar findings in a PET study of typically developing adults; ED set-shifts (and not ID set-shifts) were correlated with activation of bilateral prefrontal regions, further supporting the hypothesis that ED set-shifts (but not ID setshifts ) are dependent upon prefrontal and frontal-striatal activity. These findings are also consistent with other imaging work that reports PFC circuitry in ED set-shifting (Konishi et al., 1998, 1999, 2002; Smith, Taylor, Brammer, & Rubia, 2004; Watson et al., 2006). "
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    ABSTRACT: Neuropsychological models of frontal lobe functioning have led to a greater appreciation of the dissociations among various aspects of executive functions. Theories of executive function have been proposed to account, at least in part, for the unique social and emotional difficulties experienced by individuals with Asperger's syndrome (AS). Given the paucity of research regarding the neural correlates of executive function in AS, this investigation research involves an examination of a well-established measure of executive, fronto-striatal function in young adults with AS. Findings provide preliminary evidence to support a specific type of executive dysfunction and in particular, extradimensional or conceptual set-shifting difficulties in individuals with AS that implicates prefrontal cortex and frontal-striatal function.
    Research in Autism Spectrum Disorders 11/2013; 7(12):1631-1637. DOI:10.1016/j.rasd.2013.09.009 · 2.96 Impact Factor
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