Functional disconnection of the medial prefrontal cortex and subthalamic nucleus in attentional performance: evidence for corticosubthalamic interaction

Abstract

The present study used a disconnection procedure to test whether the medial prefrontal cortex (mPFC) and the subthalamic nucleus (STN) were functional components in a common neural system that controlled continuous performance in a test of sustained and divided visual attention. Animals with disconnected lesions of the mPFC and STN in contralateral hemispheres were severely impaired in several aspects of performance, including discriminative accuracy, increased perseveration, and slowed response latencies during postoperative testing. These deficits persisted throughout the entire experimental test period. Increasing the stimulus duration alleviated the accuracy deficit but failed to improve speed of responding or reduce perseverative responses. These deficits were in marked contrast to animals with combined mPFC and STN lesions made on the ipsilateral side, which produced behavior not different from that of sham controls. Rats with unilateral lesions of either structure alone were also impaired in terms of accuracy and perseveration. These data suggest that some of the deficits observed after bilateral STN lesions (attention and perseveration) may be attributable to a disrupted corticosubthalamic projection. This study provides direct evidence that performance in tasks that require optimal attentional and executive control relies on a corticosubthalamic interaction within the neural circuitry of the basal ganglia.

Figure 1.

Diagrammatic reconstruction of coronal sections of rat brain showing the largest (black) and smallest (gray) extent of mPFC (left hemisphere) and STN (right hemisphere) lesions in the disconnected lesioned group. The numbers indicate AP coordinates relative to bregma. Atlas plates were adapted from Paxinos and Watson (1997).

Figure 2.

Effects of theDISC group (open squares), IPL group (open triangles), and sham group (closed circles) on performance of the standard baseline task on the 5CSRTT. A, Percentage of accuracy. B, Correct latency (in centiseconds). C, Premature responses. D, Perseverative responses. Mean ± SEM results are illustrated for the last four sessions of preoperative baseline (Pre-op), 12 d of postoperative testing (Post-op), and five additional baseline sessions (Baseline).

Figure 3.

Effects of manipulating the stimulus duration on task performance of sham controls (closed bars), the IPL group (open bars), and the DISC group (hatched bars). Each bar represents mean ± SEM. A, Percentage of accuracy. B, Correct latency (in centiseconds). C, Premature responses. D, Perseverative responses. Each stimulus duration was presented in a single test session.

Figure 4.

Mean ± SEM performance of sham controls (closed diamonds) and unilateral mPFC (open circles) and unilateral STN (×) lesion groups on 12 d of postoperative baseline on the 5CSRTT. A, Percentage of accuracy. B, Perseverative responses.

Figure 5.

Summary comparisons among groups for 12 postoperative baseline sessions: Sham group, open bars; unilateral mPFC (Uni mPFC) group, gray bars; unilateral STN (Uni STN) group, thick-hatched bars; IPL, closed bars; DISC group, narrow-hatched bars. Data were collapsed across session, and mean data ± SEM are presented. A, Percentage of accuracy. B, Correct latency (in centiseconds). C, Premature responses. D, Perseverative responses.