Reward stability determines the contribution of orbitofrontal cortex to adaptive behavior - PubMed (original) (raw)

Reward stability determines the contribution of orbitofrontal cortex to adaptive behavior

Justin S Riceberg et al. J Neurosci. 2012.

Abstract

Animals respond to changing contingencies to maximize reward. The orbitofrontal cortex (OFC) is important for flexible responding when established contingencies change, but the underlying cognitive mechanisms are debated. We tested rats with sham or OFC lesions in radial maze tasks that varied the frequency of contingency changes and measured both perseverative and non-perseverative errors. When contingencies were changed rarely, rats with sham lesions learned quickly and performed better than rats with OFC lesions. Rats with sham lesions made fewer non-perseverative errors, rarely entering non-rewarded arms, and more win-stay responses by returning to recently rewarded arms compared with rats with OFC lesions. When contingencies were changed rapidly, however, rats with sham lesions learned slower, made more non-perseverative errors and fewer lose-shift responses, and returned more often to non-rewarded arms than rats with OFC lesions. The results support the view that the OFC integrates reward history and suggest that the availability of outcome expectancy signals can either improve or impair adaptive responding depending on reward stability.

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Figures

Figure 1.

Figure 1.

Experimental design. a, All animals followed the same testing sequence. Coronal sections +4.2 mm, +3.7 mm, and +3.2 mm from bregma are reproduced (Paxinos and Watson, 1998), with markings indicating lesion size; black regions represent minimum lesion locations, and diagonal lines represent maximum lesion locations. All tasks took place on the eight-arm radial maze. Three arms on the radial maze served as start arms. Correct trajectories are shown as arrows to the rewarded arm (*). b, An outline of the three reversal tasks showing decreasing numbers of trials per goal before reversal from LFR to HFR.

Figure 2.

Figure 2.

Reversal frequency determines the effect of OFC lesions on learning. a, Mean ± SEM TTC was similar in sham (gray) and lesion (black) groups during initial learning. b, Overall performance (±SEM) was impaired by OFC lesions during LFR but improved during HFR. c, Sham rats performed significantly better than rats with OFC lesions during LFR. Learning was equivalent during MFR. Rats with OFC lesions performed significantly better than sham rats during HFR. d, Within-group analysis of performance on trial 2 during LFR (open bars), MFR (dashed bars), and HFR (filled bars) shows consistent improvement across tasks in rats with OFC lesions (black) but not sham rats (gray). *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 3.

Figure 3.

Reversal frequency alters the effects of OFC lesions on performance after correct or error trials. a, The sham rats (gray circles) performed better than the rats with OFC lesions (black squares) on the trial after a correct trial during LFR (**p < 0.01). b, Rats with OFC lesions (black squares) performed better than sham rats (gray circles) on the trial after errors during HFR (**p < 0.01).

Figure 4.

Figure 4.

Non-perseverative, not perseverative, errors account for performance differences between groups. a, Entering the previously rewarded arm defined a perseverative error. Entering any other non-rewarded arm defined an non-perseverative error. b, During LFR, sham rats (blue frame) made fewer total (***p < 0.001), non-perseverative (open bars, ***p < 0.001), and perseverative (filled bars, *p < 0.05) errors than rats with OFC lesions (red frame). During HFR, sham rats made more total and non-perseverative errors (***p < 0.001 for both) than rats with OFC lesions.

Figure 5.

Figure 5.

Error types differentially correlate with performance across tasks. a, Likelihood of non-perseverative errors during LFR predicted better performance during HFR (green dots). Likelihood of perseverative errors during LFR did not predict HFR performance (purple dots). b, Better performance during LFR predicted the likelihood of making perseverative errors (purple dots), but not non-perseverative errors (green dots), during HFR. Dots with frames are individual rats with OFC lesions, and dots without frames are individual rats with sham lesions.

Figure 6.

Figure 6.

OFC lesions improve performance when initial training is in an HFR task. a, During initial learning, rats with sham (gray) and OFC (black) lesion performed indistinguishably, but during the reversal learning, rats with OFC lesions performed better than controls (*p < 0.05). b, Rats with OFC lesions performed better than sham rats on trials after errors (**p < 0.01, left) but equally on trials after correct trials (right).

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