The role of the orbitofrontal cortex in the pursuit of happiness and more specific rewards

Abstract

Cues that reliably predict rewards trigger the thoughts and emotions normally evoked by those rewards. Humans and other animals will work, often quite hard, for these cues. This is termed conditioned reinforcement. The ability to use conditioned reinforcers to guide our behaviour is normally beneficial; however, it can go awry. For example, corporate icons, such as McDonald's Golden Arches, influence consumer behaviour in powerful and sometimes surprising ways, and drug-associated cues trigger relapse to drug seeking in addicts and animals exposed to addictive drugs, even after abstinence or extinction. Yet, despite their prevalence, it is not known how conditioned reinforcers control human or other animal behaviour. One possibility is that they act through the use of the specific rewards they predict; alternatively, they could control behaviour directly by activating emotions that are independent of any specific reward. In other words, the Golden Arches may drive business because they evoke thoughts of hamburgers and fries, or instead, may be effective because they also evoke feelings of hunger or happiness. Moreover, different brain circuits could support conditioned reinforcement mediated by thoughts of specific outcomes versus more general affective information. Here we have attempted to address these questions in rats. Rats were trained to learn that different cues predicted different rewards using specialized conditioning procedures that controlled whether the cues evoked thoughts of specific outcomes or general affective representations common to different outcomes. Subsequently, these rats were given the opportunity to press levers to obtain short and otherwise unrewarded presentations of these cues. We found that rats were willing to work for cues that evoked either outcome-specific or general affective representations. Furthermore the orbitofrontal cortex, a prefrontal region important for adaptive decision-making, was critical for the former but not for the latter form of conditioned reinforcement.

Figure 1. Effect of orbitofrontal lesions on pavlovian conditioning and reinforcer devaluation

Shown is the experimental timeline, with boxes linking conditioning, compound conditioning, and reinforcer devaluation phases to data from each phase. In the timeline and figures, A, B, X and Y are training cues; R1 and R2 are instrumental responses; and O1 and O2 are different flavoured sucrose pellet reinforcers. a, Responses per minute in the food cup during the first period of the conditioned stimulus (CS) (first 8 s) for A and B during pavlovian conditioning sessions. There were no effects of lesions. b, Responses per minute in the food cup during the first cue period, for AX and BY during compound pavlovian conditioning sessions. The timing of the two probe tests and the pre-devaluation conditioned reinforcement (CRf) testing are indicated by arrows. There were no effects of lesions. c, Food pellets consumed during the final two days of devaluation (days 5 and 6) for control (open bar) and lesion (filled bar) groups. There were no effects of lesions. D, devalued pellet; ND, non-devalued pellet. Error bars denote s.d.

Figure 2. Effect of orbitofrontal lesions on conditioned reinforcement for a fully conditioned A cue, for a blocked X cue, and for the partially blocked Y cue before and after reinforcer devaluation

Shown is the experimental timeline linked to data from each conditioned reinforcement (CRf) test. In the timeline and figures, A, B, X and Y are training cues; R1 and R2 are instrumental responses; and O1 and O2 are different flavoured sucrose pellet reinforcers. a–d, Lever pressing for A versus X, or Y versus X, in control (open bars) and lesioned (filled bars) rats before (a, b) and after (c, d) devaluation. Lesions diminished responding for Y before devaluation (a, b), controls diminished lever pressing for Y after devaluation (c, d). Lever pressing is averaged across two 30-min sessions in each figure. Asterisks indicate significance at P < 0.05 on post-hoc contrast testing; the grey numbers indicate the ratio of responding on the two levers for each significant comparison. NS, not significant. Error bars denote s.d.

Figure 3. Effect of orbitofrontal lesions on pavlovian conditioned responding after transreinforcer blocking in extinction probe tests

Shown is the experimental timeline linked to data from the blocking probe tests. In the timeline and figures, A, B, X and Y are training cues; R1 and R2 are instrumental responses; and O1 and O2 are different flavoured sucrose pellet reinforcers. Responses per minute at the food cup are shown individually for each of six unrewarded presentations of A, B, X and Y (small black (lesioned) and white (control) boxes) and also averaged over all six presentations (large grey (lesioned) and white (control) bars). Lesions had no effect on responding for A, B or X, but significantly diminished responding for Y. Error bars represent s.d.