A new perspective on the role of the orbitofrontal cortex in adaptive behaviour

Abstract

The orbitofrontal cortex (OFC) is crucial for changing established behaviour in the face of unexpected outcomes. This function has been attributed to the role of the OFC in response inhibition or to the idea that the OFC is a rapidly flexible associative-learning area. However, recent data contradict these accounts, and instead suggest that the OFC is crucial for signalling outcome expectancies. We suggest that this function--signalling of expected outcomes--can also explain the crucial role of the OFC in changing behaviour in the face of unexpected outcomes.

Figure 1. Showing orbitofrontal involvement in flexible, adaptive behaviour in rats using an odour discrimination reversal task

The events in a simple odour discrimination reversal task that demonstrates the involvement of the orbitofrontal cortex in flexible, adaptive behaviour. Rats sample an odour from a port. After sampling, they decide whether to respond at a nearby fluid well. One odour predicts a tasty sucrose solution, whereas a second odour predicts an unpleasant-tasting quinine solution. As illustrated in the top panel, rats rapidly learn to discriminate between the odours, drinking from the fluid well after sampling the sucrose-predicting odour but withholding that response after sampling the quinine-predicting odour. After this has been learned, the odour–outcome associations can be reversed, such that the sucrose-predicting odour comes to predict quinine and vice versa. This is illustrated in the bottom panel. Initially rats respond on the basis of what they have learned previously. However, normal rats rapidly recode these associations (a) and inhibit their old response patterns in favour of new ones (b); rats with damage to the orbitofrontal cortex fail to change their behaviour as rapidly.

Figure 2. Stylized plots of reward-responsive neurons in the orbitofrontal cortex

a | In discrimination learning tasks, neurons in the rat orbitofrontal cortex (OFC) initially fire in response to either the rewarding reinforcer (for example, sucrose) or the aversive reinforcer (for example, quinine) (dark blue line). After a number of trials the neurons also start to fire in anticipation of the reinforcer (red line). Finally, they also come to fire in response to cues that predict the reinforcer (purple line). b | These OFC neurons do not stop firing in response to the reward, even after many trials. Moreover, their firing is not stronger in response to an unexpected reward or weaker in response to the omission of a reward left panel). In this respect, OFC neurons are unlike dopamine (DA) neurons in the ventral tegmental area (VTA), which are also reward responsive but which fire more strongly in response to unexpected rewards and decrease firing when an expected reward is not delivered (right panel). Based on data from REFS –.

Figure 3. The proposed role of the orbitofrontal cortex in flexible, adaptive behaviour

A summary of several proposals reviewed in the text for explaining the role of the orbitofrontal cortex (OFC) in facilitating reversal learning. At the top is the historical proposal that output from the OFC directly inhibits ‘pre-potent’ responses and is therefore crucial for reversal learning. Below is the more recent idea that the OFC functions as a highly flexible associative reference table to directly guide correct responding and so is vital for reversal learning. At the bottom is our alternative proposal that the OFC is crucial for reversal learning because it drives associative learning in other structures. According to this proposal, the OFC does this by supporting the generation of teaching signals (for example, by the ventral tegmental area (VTA)) when actual outcomes do not match signals from the OFC regarding expected outcomes. BLA, basolateral amygdala; mPFC, medial prefrontal cortex.