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

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.

Acute Δ9-Tetrahydrocannabinol-Induced Deficits in Reversal Learning: Neural Correlates of Affective Inflexibility

“…However, the cognitive tasks employed in these studies involve several different cognitive components, and inflexible responding may therefore arise as a consequence of an impairment at one of several levels of cognitive processing (Rogers et al, 2000). The componential analysis provided in the present study suggests that acute administration of THC results in impairments in affective flexibility, rather than in the ability to shift strategy or set per se.…”

“…These processes are also anatomically dissociable; lesions of the monkey lateral PFC (Dias et al, 1996a(Dias et al, , b, 1997 and the equivalent prelimbic and infralimbic regions of the rat medial frontal cortex (Birrell and Brown, 2000) markedly disrupt extradimensional attentional set shifting ability, while lesions of the orbitofrontal cortex (OFC) selectively impair reversal learning in both species (Butter, 1969;Dias et al, 1996aDias et al, , 1997Ferry et al, 2000;Iversen and Mishkin, 1970;Jones and Mishkin, 1972;McAlonan and Brown, 2003;Schoenbaum et al, 2002). Recently, studies have also emphasized a role for the ventral striatum in transforming reversed stimulus reward contingencies into altered behavioral responses (Cools et al, 2002(Cools et al, , 2004Crofts et al, 2001;Divac et al, 1967;Monchi et al, 2001;Rogers et al, 2000;Stern and Passingham, 1995).…”

Brain imaging of the central executive component of working memory

“…Moreover, they also indicate that similar prefrontal areas are activated by tasks requiring executive processes which at a first sight are quite different. For example, the middle prefrontal gyrus (BA 9/46) was found in manipulation [30,40,98] and updating [103,124] tasks as well as in dual-task coordination [39], inhibition processes [26,31] and shifting processes [102]. Furthermore, the activity of that region was directly linked to the memory load, as demonstrated by Braver et al [17] and Cohen et al [28] using parametric design studies.…”

“…After a pre-determined number of correct responses, the discrimination rule changes and participants have to shift from the processing of the relevant perceptual dimension to a new one that was previously considered as irrelevant. Using TEP, Rogers et al [102] explored cerebral areas involved when participants have to shift from the processing of one stimulus dimension to another. Two conditions were administered: intra-dimensional shift condition, requiring the application of a previously learned discrimination decision rule to a new set of stimuli; and extra-dimensional shift condition, in which participants have to identify a new discrimination rule, again with novel test stimuli.…”

Reduced brain connectivity and mental flexibility in mild traumatic brain injury

“…Mental in flexibility is one of the cognitive complaints experienced in mTBI14 and manifests as a tendency to perseverate or “become stuck.” The neural underpinnings of mental flexibility have been well studied using the Wisconsin Card Sort Task,29 and areas in prefrontal, frontal, and posterior cortical regions have been implicated using both fMRI30, 31, 32, 33, 34, 35, 36 and MEG 37, 38, 39. Our group has designed a simpler task aimed at probing the core “shifting” aspect of mental flexibility and we have optimized this for MEG 40…”