Article

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

ABSTRACT

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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    • "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]. "

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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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