Differential responses in human striatum and prefrontal cortex to changes in object and rule relevance

Abstract

Event-related functional magnetic resonance imaging was used to measure blood oxygenation level-dependent responses in 16 young healthy human volunteers during performance of an attentional switching task. The task allowed the separate investigation of lower-order switching between concrete objects and higher-order switching between abstract task rules. Significant signal change in the ventral striatum was demonstrated on trials when subjects switched between objects but not when subjects switched between abstract task rules. In contrast, signal change in the lateral prefrontal cortex (PFC) was observed during all switch trials. The switch-related responses were not contaminated by task difficulty, because the greatest signal change was observed during the relatively easy switch trials, which required both lower-order and higher-order switching at the same time. The present data suggest that mechanisms of inhibitory response control in frontostriatal systems are organized according to distinct levels of abstraction. Specifically, the response selection computation carried by the ventral striatum, which projects to the orbitofrontal cortex and the medial PFC, is restricted to the transformation of concrete stimulus exemplar information into motor responses, whereas the adaptive function of the lateral PFC extends to the transformation of abstract task-rule representations into action.

Figure 1.

Task design. An example sequence of trials is displayed, with the arrow indicating the correct response. The yellow (here, light gray) stimulus windows cued the subject to choose the same object as on the previous trial. The blue (here, dotted dark gray) stimulus windows cued the subject to switch to the other object. Examples of all four trial types are shown.

Figure 2.

Regions of interest. The ventral striatum is shown in black, and the dorsal striatum is shown in white. [This figure is based on work by Tzourio-Mazoyer et al. (2002)].

Figure 3.

Signal change in the striatum during object switching. A, Contrast images (object-switch trials minus rule-switch trials) with continuous activation values representing percent signal change are shown as a transparent color map superimposed on the MNI template brain (individual brain considered most typical of the 305 brains used to define the MNI standard). B, Contrast images (object–rule-switch trials minus rule-switch trials) with continuous activation values (as shown previously).

Figure 4.

Signal change relative to baseline nonswitch trials. A, Percent signal change in the left ventral striatum during object-, rule-, and object–rule-switch trials relative to nonswitch trials. Signal change in the left VS was significantly increased during the object-switch events relative to the rule-switch events (see Results) and also during the combined object–rule-switch events relative to the rule-switch events (left VS, t = 3.31, p = 0.002; right VS, t = 2.36, p = 0.02), but the increase during the combined object–rule-switch trials relative to the object-switch trials did not reach significance according to our criterion (left VS, t = 2.01, p = 0.03; right VS, t = 1.9, p = 0.04). Signal change in the dorsolateral PFC (B) (Talairach coordinates, x, y, z = –48, 24, 21) and the ventrolateral PFC (C) (x, y, z = –30, 27, 6) during object-, rule-, and object–rule-switch trials relative to nonswitch trials are shown. Error bars represent SEs of the difference.

Figure 5.

Switch costs. Switch costs were calculated by subtracting performance on baseline nonswitch trials from performance on the three switch trials. RTs in milliseconds and errors and omissions are shown. Error bars represent SEs of the difference.