Remembering with gains and losses: effects of monetary reward and punishment on successful encoding activation of source memories

Abstract

The motivation of getting rewards or avoiding punishments reinforces learning behaviors. Although the neural mechanisms underlying the effect of rewards on episodic memory have been demonstrated, there is little evidence of the effect of punishments on this memory. Our functional magnetic resonance imaging (fMRI) study investigated the effects of monetary rewards and punishments on activation during the encoding of source memories. During encoding, participants memorized words (item) and locations of presented words (source) under 3 conditions (Reward, Punishment, and Control). During retrieval, participants retrieved item and source memories of the words and were rewarded or penalized according to their performance. Source memories encoded with rewards or punishments were remembered better than those without such encoding. fMRI data demonstrated that the ventral tegmental area and substantia nigra and nucleus accumbens activations reflected both the processes of reward and punishment, whereas insular activation increased as a linear function of punishment. Activation in the hippocampus and parahippocampal cortex predicted subsequent retrieval success of source memories. Additionally, correlations between these reward/punishment-related regions and the hippocampus were significant. The successful encoding of source memories could be enhanced by punishments and rewards, and interactions between reward/punishment-related regions and memory-related regions could contribute to memory enhancement by reward and/or punishment.

Keywords: functional magnetic resonance imaging; punishment; reward; source memory.

Figure 1.

Experimental design of encoding and retrieval blocks. (a) During encoding, Japanese words were presented on the left or right side of the screen in 3 different font types. Participants were instructed to memorize the words (item) and on which side (left or right) they were presented (source) by judging font types. The cues indicated the 3 different conditions (Reward, Punishment, and Control). Participants were told that they would be rewarded when they could remember item and/or source encoded in the Reward condition, and that they would be penalized when they could not remember item and/or source encoded in the Punishment condition in the subsequent retrieval blocks. (b) During retrieval, old and new words were randomly presented in the center of the screen. Participants were required to judge whether the words had been previously presented and on which side they were presented during encoding. All labels were actually presented in Japanese. English is used here for illustration purposes only.

Figure 2.

Mean proportion of retrieval accuracy for both the IWS and IO memories in the Reward, Punishment, and Control conditions. Error bars represent standard error. *P < 0.05.

Figure 3.

Activation images and activation profiles in reward-/punishment-related regions. Regions associated with both rewards and punishments were identified in the right VTA/SN and right NA regions. The right insular activation reflected a linearly increasing function of punishment. The numbers of each point show the mean effect size (SE) in each condition.

Figure 4.

Activation images and activation profiles in encoding-related regions predicting successful retrieval of IWS memories. The right hippocampus and left PHC regions showed increasing activation associated with the subsequently successful retrieval of IWS memories. IWS: successful encoding of item with source memories, IO: successful encoding of IO memories, ME: missed encoding of memories. The numbers of each point show the mean effect size (SE) in each condition.

Figure 5.

Correlation patterns between activations in the reward-/punishment-related and memory-related hippocampal regions and activation pattern in the hippocampal region. (a) Correlations between the reward-/punishment-related VTA and NA regions and the memory-related hippocampal region. (b) Correlation between the punishment-related insular and the memory-related hippocampal regions. Gray lines represent significant correlations between reward-/punishment-related and memory-related hippocampal regions (P < 0.05). (c) Right hippocampal activation, which reflected the successful encoding of IWS memories, was also affected by a reward/punishment factor, where the activation was greater during the successful encoding of IWS memories under the Reward and Punishment conditions than the Control condition. Error bars represent standard errors. *P < 0.05.