Punishing an error improves learning: the influence of punishment magnitude on error-related neural activity and subsequent learning

Abstract

Punishing an error to shape subsequent performance is a major tenet of individual and societal level behavioral interventions. Recent work examining error-related neural activity has identified that the magnitude of activity in the posterior medial frontal cortex (pMFC) is predictive of learning from an error, whereby greater activity in this region predicts adaptive changes in future cognitive performance. It remains unclear how punishment influences error-related neural mechanisms to effect behavior change, particularly in key regions such as pMFC, which previous work has demonstrated to be insensitive to punishment. Using an associative learning task that provided monetary reward and punishment for recall performance, we observed that when recall errors were categorized by subsequent performance--whether the failure to accurately recall a number-location association was corrected at the next presentation of the same trial--the magnitude of error-related pMFC activity predicted future correction. However, the pMFC region was insensitive to the magnitude of punishment an error received and it was the left insula cortex that predicted learning from the most aversive outcomes. These findings add further evidence to the hypothesis that error-related pMFC activity may reflect more than a prediction error in representing the value of an outcome. The novel role identified here for the insular cortex in learning from punishment appears particularly compelling for our understanding of psychiatric and neurologic conditions that feature both insular cortex dysfunction and a diminished capacity for learning from negative feedback or punishment.

Figure 1.

The spatial paired associated learning task used in the present study, represented by the screen transitions for the encoding and recall phases of the task. Each block of trials began with an encoding phase that presented the two-digit number associated with each location (2000 ms) and an intertrial interval display (1000 ms). All eight number–location associations were presented once during the encoding phase and were immediately followed by the recall phase. A single trial in the recall phase began by highlighting a location in yellow to cue the participant to respond with the two-digit number they associated with the location. Following a variable interstimulus delay, feedback was provided that consisted of presenting the accuracy of the response (red background for an error, blue for correct) and the magnitude of the reward/punishment (an Australian 5 or 50¢ coin). Following a second variable interstimulus display, participants were presented with the actual number associated with the location to enable encoding of the correct response (re-encoding epoch), regardless of prior recall accuracy.

Figure 2.

Method used to classify corrected and repeated errors. Feedback for a participant's response involved presentation of the correct number on either a red background, indicating an error, or a blue background, indicating an accurate recall response. Categorization as either a corrected or repeated error was determined by the participant's performance for the same trial during the next round. In the corrected error example, the participant incorrectly recalled the digits associated with the top left location (responding with 33 rather than 44) during round 1, but correctly recalled these digits during round 2 and so the initial round 1 error is categorized as a corrected error. In the repeated error example, the participant incorrectly responded to the presentation of the top right location during both round 1 and 2, and therefore the initial error is categorized as a repeated error. Dots represent the intervening trials.

Figure 3.

A, Three-dimensional rendering from the axial perspective of the medial prefrontal cortex functional derived region of interest (MNI coordinates: x = −2; y = 0; z = 47) activated during the feedback epoch for recall errors. Cluster activity was determined relative to averages across intertrial delay periods. B, Estimates of mean percentage change in BOLD activity during the feedback epoch for corrected and repeated errors receiving either 5 or 50¢ monetary punishment.

Figure 4.

A–C, Three-dimensional rendering of the right hippocampal functionally derived region of interest (MNI coordinates: x = 37, y = −31, z = −9) activated during the re-encoding epoch for recall errors, from sagittal (A), axial (B), and coronal (C) perspectives. BOLD activity estimates were derived for each individual trial from the pMFC and left insula clusters during feedback and the hippocampus cluster during re-encoding. D, The correlation coefficient for these paired values across all trials was calculated to estimate the relationship. A significant positive correlation was identified between pMFC and hippocampal cortex (HC) activity estimates (mean intraindividual correlation, r = 0.22; range, r = −0.16–0.51; p = 8.6135 × 10⁻¹⁴), and left insula and hippocampal activity estimates (mean intraindividual correlation, r = 0.18; range, r = −0.11–0.52; p = 7.1 × 10⁻²¹) and the intraindividual correlation value is plotted in D for each participant.

Figure 5.

A, Three-dimensional rendering, from both the coronal and sagittal perspective, of the left anterior insula cortex functionally derived region of interest (MNI coordinates: x = −41, y = 8, z = 7) activated during the feedback epoch for recall errors. Cluster activity was determined relative to baseline activity averaged across intertrial delay periods. B, Estimates from the feedback epoch of mean percentage change in BOLD activity during corrected and repeated errors receiving either 5 or 50¢ monetary punishment. C, Pearson correlation coefficient scatterplot of the significant relationship between feedback epoch activity for corrected errors in the pMFC and left insula cortex regions. L, Left; R, right.