Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex

Abstract

To examine possible heterogeneity of function within the ventral regions of the rodent frontal cortex, the present study compared the effects of excitotoxic lesions of the orbitofrontal cortex (OFC) and the infralimbic cortex (ILC) on pavlovian autoshaping and discrimination reversal learning. During the pavlovian autoshaping task, in which rats learn to approach a stimulus predictive of reward [conditional stimulus (CS+)], only the OFC group failed to acquire discriminated approach but was unimpaired when preoperatively trained. In the visual discrimination learning and reversal task, rats were initially required to discriminate a stimulus positively associated with reward. There was no effect of either OFC or ILC lesions on discrimination learning. When the stimulus-reward contingencies were reversed, both groups of animals committed more errors, but only the OFC-lesioned animals were unable to suppress the previously rewarded stimulus-reward association, committing more "stimulus perseverative" errors. In contrast, the ILC group showed a pattern of errors that was more attributable to "learning" than perseveration. These findings suggest two types of dissociation between the effects of OFC and ILC lesions: (1) OFC lesions impaired the learning processes implicated in pavlovian autoshaping but not instrumental simultaneous discrimination learning, whereas ILC lesions were unimpaired at autoshaping and their reversal learning deficit did not reflect perseveration, and (2) OFC lesions induced perseverative responding in reversal learning but did not disinhibit responses to pavlovian CS-. In contrast, the ILC lesion had no effect on response inhibitory control in either of these settings. The findings are discussed in the context of dissociable executive functions in ventral sectors of the rat prefrontal cortex.

Figure 1.

Line drawing of apparatus used for autoshaping task (A) and visual discrimination discrimination task (B): A, pressure-sensitive floor panel; B, food magazine; C, pellet dispenser; D, computer graphic stimuli; E, video display unit (touch screen); F, Perspex mask with response windows and shelf.

Figure 2.

Diagrammatic reconstructions of coronal sections (Paxinos and Watson, 1997) showing the largest (black shading) and smallest (gray shading) extent of the OFC lesion from experiment 1a (A) and the ILC lesion from experiment 1c (B). Numbers in each section indicate the AP level anterior to bregma. AID, Dorsal agranular insular cortex; AIV, ventral agranular insular cortex; Cg2, cingulate cortex, area 2; DLO, dorsolateral orbital cortex.

Figure 3.

Mean ± SEM difference scores of sham controls and animals with OFC lesions on discriminated approach: A, acquisition; B, omission test.

Figure 4.

Mean ± SEM performance of ILC on acquisition of discriminated approach (autoshaping): A, number of approaches to the CS⁺ and CS^- for last five blocks of trials; B, difference scores.

Figure 5.

Performance of sham controls (white bars) and OFC lesion (black bars) group on visual discrimination and reversal learning. Each error bar represents mean ± SEM: A, errors committed during correction trials; B, errors committed during noncorrection trials; C, stimulus perseverative errors committed before chance performance; D, learning errors committed after chance performance.

Figure 6.

Mean ± SEM discrimination sensitivity (d′ score) and responsivity (c score) index for sham controls (white bars) and OFC lesion (black bars) groups for each reversal during the first three sessions: A, d′ score for reversal 1; B, d′ score for reversal 2; C, c score for reversal 1; D, c score for reversal 2.

Figure 7.

Mean ± SEM performance of sham controls (white bars) and ILC lesion (hatched bars) group on visual discrimination and reversal learning: A, errors committed during correction trials; B, errors committed during non-correction trials; C, stimulus perseverative errors committed before chance performance; D, learning errors committed after chance performance.