Orbitofrontal cortex and representation of incentive value in associative learning

Abstract

Clinical evidence indicates that damage to ventromedial prefrontal cortex disrupts goal-directed actions that are guided by motivational and emotional factors. As a consequence, patients with such damage characteristically engage in maladaptive behaviors. Other research has shown that neurons in the corresponding orbital region of prefrontal cortex in laboratory animals encode information regarding the incentive properties of goals or expected events. The present study investigates the effect of neurotoxic orbitofrontal cortex (OFC) lesions in the rat on responses that are normally influenced by associations between a conditioned stimulus (CS) and the incentive value of reinforcement. Rats were first trained to associate a visual CS with delivery of food pellets to a food cup. As a consequence of learning, rats approached the food cup during the CS in anticipation of reinforcement. In a second training phase, injection of LiCl followed consumption of the food unconditioned stimulus (US) in the home cage, a procedure used to alter the incentive value of the US. Subsequently, rats were returned to the conditioning chamber, and their responding to the CS in the absence of the food US was tested. Lesions of OFC did not affect either the initial acquisition of a conditioned response to the light CS in the first training phase or taste aversion learning in the second training phase. In the test for devaluation, however, OFC rats exhibited no change in conditioned responding to the visual CS. This outcome contrasts with the behavior of control rats; after devaluation of the US a significant decrease occurred in approach to the food cup during presentation of the CS. The results reveal an inability of a cue to access representational information about the incentive value of associated reinforcement after OFC damage.

Fig. 1.

Photomicrographs and schematics showing the region of OFC damage. A, Photomicrographs showing a coronal section (anteroposterior, +2.7) from a control brain (left panel) and a lesioned brain (right panel). Note the neuronal loss, accompanied by gliosis, in the ventrolateral and lateral orbital regions and in agranular insular cortex in the lesioned brain. The region of cell loss ends at the medial orbital area and extends dorsally somewhat into parietal cortex. B, Drawings show the approximate extent and range of the lesions that were included in the experimental group. The boundaries of the minimal lesion (black fill) and the maximal lesion (diagonal fill) are shown to indicate of the range of damage. The approximate size of the lesion (crossed fill) in a subject that is representative of average lesion size is also shown [drawings adapted from Swanson (1992)]. Damage was confined to portions of OFC rostral to the genu of the corpus callosum to avoid gustatory input to posterior agranular insular cortex (Saper, 1982; Krushel and Van Der Kooy, 1988).

Fig. 2.

Data are shown for each phase of the behavioral experiment. Squares represent control groups, and circles represent the lesioned groups. All groups acquired conditioned food cup responses in phase 1, as shown in the panel on the left. In phase 2, the groups represented byfilled symbols received unpaired food and LiCl;open symbols represent groups that had paired presentations of these events. As shown in the presentation of the phase 3 devaluation test data, the control group for which food was devalued (open bar on the left) reduced conditioned responding relative to the unpaired control group (solid bar). In contrast, the lesioned groups exhibited conditioned responses that did not differ as a function of devaluation. See Materials and Methods for details of statistical analyses.