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: 4.69). 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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Available from: Thomasin C. Andrews, Aug 28, 2014
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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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    • "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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    • "Oddball tasks measure specific aspects of cognitive control, a construct that subsumes working memory, inhibition, and mental flexibility abilities that share the purpose of engaging, disengaging, and reengaging with the environment to guide behavior (Lezak 1995). In the context of oddball tasks, prefrontal activation to target events is thought to reflect the context-dependent strategic control of behavior (Huettel et al. 2004; Casey et al. 2001), dynamic changes in behavioral response strategies (Huettel and McCarthy 2004), as well as set shifting and inhibitory control (Rubia et al. 2001; Konishi et al. 1999; Rogers et al. 2000), whereas striatal (i.e., caudate nucleus and putamen) activation has been implicated in planning and the execution of self-generated novel actions (Monchi et al. 2006). Our research group has conducted a series of studies examining frontostriatal brain function during oddball tasks in individuals with ASDs. "
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