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

University of Cambridge, Cambridge, England, 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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    • "Concurring with this view, these deficits in PD are redressed by dopamine replacement (Shook et al., 2005; Hood et al., 2007; MacDonald et al., 2011). Finally, many neuroimaging experiments have also shown preferential activity in DS at the time of flexible decision-making and response selection during conflict (Grinband et al., 2006; Monchi et al., 2001; Monchi et al., 2006; Rogers et al., 2000; van Schouwenburg et al., 2010; Ali et al., 2010). A generally unacknowledged problem with the conclusions about DS drawn from these investigations is that as cognitive control demands of a task are increased, the cognitive effort required correspondingly increases . "
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    ABSTRACT: Whether the dorsal striatum (DS) mediates cognitive control or cognitive effort per se in decision-making is unclear given that these effects are highly correlated. As the cognitive control requirements of a neuropsychological task intensify, cognitive effort increases proportionately. We implemented a task that disentangled cognitive control and cognitive effort to specify the particular function DS mediates in decision-making. Sixteen healthy young adults completed a number Stroop task with simultaneous blood-oxygenation-level-dependent response (BOLD) measurement using functional magnetic resonance imaging. Participants selected the physically larger number of a pair. Discriminating smaller physical size differences between a number pair increases cognitive effort, but does not demand greater cognitive control. We also investigated the effect of conflict between the physical and numerical dimensions of targets (e.g.,2 6). Selections in this incongruent case are more cognitively effortful and require greater cognitive control to suppress responding to the irrelevant dimension. Enhancing cognitive effort or control increases errors and response times. Despite similar behavioural profiles, our aim was to determine whether DS simply indexes cognitive effort versus specifically mediates cognitive control, using the same data set. As expected, behavioural interference effects occurred for both enhanced cognitive control and/or cognitive effort conditions. Despite similar degrees of behavioural interference, DS BOLD signal only correlated with interference arising due to increased cognitive control requirements in the incongruent case. DS was not preferentially activated for discriminations of smaller relative to larger physical size differences between number pairs, even when using liberal statistical criteria. However, our incongruent and physical size effects conjointly activated regions related to effortful processing (e.g., ACC). We interpret these findings as support for the increasingly-accepted notion that DS mediates cognitive control specifically and does not simply index cognitive effort per se. Copyright © 2015. Published by Elsevier Inc.
    Full-text · Article · Apr 2015 · NeuroImage
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    • "Previous research has found impairments in patients with lesions in the prefrontal cortex[39]and fMRI studies have supported these findings, linking the prefrontal cortex to set shifting[40,41]. There has been some speculation that the basal ganglia is also involved in the WCST since impairments have also been seen in Parkinson's disease patients[42]. "

    Full-text · Article · Aug 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.
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