Dissociating Striatal and Hippocampal Function Developmentally with a Stimulus–Response Compatibility Task

Abstract

The current study examined the development of cognitive and neural systems involved in overriding a learned action in favor of a new one using a stimulus-response compatibility task and functional magnetic resonance imaging. Eight right-handed adults (mean age, 22-30 years), and eight children (7-11 years) were scanned while they performed a task. Both children and adults were less accurate for incompatible stimulus-response mappings than compatible ones; the children's performance was significantly worse. The comparison of the incompatible and compatible conditions showed large volumes of activity in the ventral prefrontal cortex, ventral caudate nucleus, thalamus, and hippocampus. Striatal activity correlated with the percentage of errors in overriding the old stimulus-response association. The hippocampal activity correlated with the reaction time to make a response to a new stimulus-response mapping that required the reversal of a prior association between a stimulus and a response location. Developmental differences were observed in the volume of striatal/pallidal and hippocampal/parahippocampal activity in that these regions were larger and extended more ventrally in children relative to adults. These results suggest that with maturation and learning, projections to and from these regions may become more refined and focal. Moreover, these findings are consistent with the role of ventral frontostriatal circuitry in overriding habitual and well learned actions and hippocampal systems in learning and reversing associations between a given stimulus and spatial location. Key words: development; basal ganglia; hippocampus; imaging; learning; fMRI; childrenThe ability to override competing actions is a key component of cognitive functioning (Kahneman et al., 1983;Baddeley, 1986;Shallice, 1988;Cohen and Servan-Schreiber, 1992;Desimone and Duncan, 1995); it becomes more efficient with age (Harnishfeger and Bjorkland, 1993). In other words, immature cognition is characterized by greater susceptibility to interference from competing actions (Diamond, 1990;Brainerd and Reyna, 1993;Dempster, 1993;Casey et al., 2001Casey et al., , 2002Munakata and Yerys, 2001), as evidenced in children when performing Stroopinterference tasks (Tipper et al., 1989), card sorting (Zelazo et al., 1996;Munakata and Yerys 2001), and go-no-go tasks (Luria, 1961; Casey et al., 1997a,b;Vaidya et al., 1998). In all cases, children have more difficulty making the correct response when there is interference from competing response alternatives.Overriding well learned actions in favor of new ones and the development of neural subsystems underlying this ability is the focus of this paper. In essence, how does the less mature system recruit brain regions when making a new response to a given stimulus relative to making a well learned response to that same stimulus (i.e., stimulus-response incompatibility)? This ability involves both overriding an old association while simultaneously learning a new one. The ability to shift between behavioral sets has...

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