Elsevier

NeuroImage

Volume 54, Issue 2, 15 January 2011, Pages 1669-1676
NeuroImage

Projecting memories: The role of the hippocampus in emotional mentalizing

https://doi.org/10.1016/j.neuroimage.2010.08.057Get rights and content

Abstract

Humans have a striking tendency to use past autobiographical events to understand their own behavior. However, it is unknown if we use our own memories to understand others.

To assess the role of autobiographical memory in mentalizing we examined the contribution of memory structures, specifically the hippocampus, to emotional judgment of others. Subjects were scanned while making emotional judgments regarding themselves, and protagonists deemed similar to or dissimilar from themselves. Results indicated a significant correlation between rating of the self and the similar protagonists, particularly for the events subjects recalled from their past. Furthermore, we found an interaction between similarity and recollection so that only for events subjects recalled from their past, the hippocampus reacted differently for judgments regarding the self versus dissimilar others, but not for self versus similar others. These results suggest that people actually use their own repertoire of memories and project internal self knowledge while making emotional judgments regarding others. It is speculated that mentalizing is modulated by memories of similar past events and depends on the protagonist we face.

Research Highlights

► People use their own autobiographical memories to understand others (mentalizing). ► The hippocampus reacts differently for judgments regarding the self versus dissimilar others, but not for self versus similar others, only for events subjects recall from their past. ► We use our own repertoire of memories and project internal self knowledge while making emotional judgments regarding others. ► Mentalizing is modulated by memories of similar past events and by perceived similarity between ourselves and others.

Introduction

The famous biblical passage “You shall not oppress the stranger, for you know the soul of the stranger, having been strangers in the land of Egypt.” (Exodus 23:9) suggests that people should use their own life experience while judging other individuals. Indeed, a remarkable characteristic of human nature is the ability to consider past events when judging others.

The ability to recognize that others have independent experiences, desires and intentions is termed mentalizing (Amodio and Frith, 2006). Recent neuroimaging studies demonstrate that a similar set of brain regions that includes the medial prefrontal cortex (MPFC) and aspects of lateral and medial parietal cortex participates in both mentalizing and episodic memory (Mitchell, 2009). Moreover, accumulating data suggest that self-projection (the ability to shift perspective from the immediate present to alternative perspectives), remembering the past, and mentalizing are based on the same core brain networks (Buckner and Carroll, 2007), suggesting that these processes share similar mechanisms.

Episodic autobiographical memory (AM), our ability to recall knowledge of our past that occurred at one specific point in time, has been shown to involve a widespread left-predominant cerebral network incorporating the medial temporal lobe (MTL) and the MPFC (Addis et al., 2004a). The MTL is known for its role in declarative memory, which includes episodic memory (Tulving and Markowitsch, 1998). Lesion studies demonstrate that damage to the MTL, including the hippocampus, may result in failure to anticipate future events together with an inability to retrieve past events (Tulving, 1985, Klein et al., 2002, Rosenbaum et al., 2000). Thus, it could be concluded that the MTL, which has long been considered crucial for remembering the past, serves also to provide building blocks for self-projection and future simulation (Addis et al., 2007, Schacter et al., 2007).

One plausible hypothesis that emerges from this line of studies is that AM and mentalizing rely on a common set of processes by which past experiences are used to understand events happening to the self as well as to others.

The relationship between mentalizing and AM has been first described in individuals with schizophrenia (Corcoran and Frith, 2003), but the specific nature of these relations in healthy individuals has yet to be characterized.

Three potential models may describe the possible relationship between metalizing and AM. The first possible relationship between mentalizing and AM is that of dependence. A dependence model may propose that mentalizing is based on AM and that mentalizing requires self-projection, which is based on memory of our past experiences. According to this formulation impairment in AM will result in impaired mentalizing, as reported in patients with schizophrenia (Corcoran and Frith, 2003). Findings from a seminal lesion study, however, have put this possibility in question by showing that performance on tasks that involve mentalizing is not affected by amnesia (Rosenbaum et al., 2007). Rosenbaum and her colleagues demonstrated that despite losing the ability to consciously recollect personal history, amnesic patients exhibit intact mentalizing abilities. This study appears to contradict the dependence model and support a model of exclusivity, as it suggests that mentalizing and AM rely on separate, independent systems, and that damage to one system does not affect the other.

Yet, a third possibility is that AM modulates mentalizing depending on the situation. For example, one possibility is that mentalizing about a certain situation occurring to a protagonist (e.g. Joe lost his wallet) is modulated by AM only when we actually recall having experienced a similar situation (I recall losing my wallet). Additionally, it is possible that the participation of AM in mentalizing depends on the protagonist we face (similar vs. dissimilar to ourselves).

While previous studies have examined the relationship between general AM and mentalizing abilities, here we compare mentalizing about events that subjects remember vs. events that subjects do not remember happening to them in the past.

To test the hypothesis that AM participates in mentalizing, we assessed the role of memory in emotional judgments regarding the self and others. We created a novel slow event-related fMRI experimental design in which emotional judgment regarding self and others was examined in the context of daily events. Prior to scanning, each subject was introduced to a set of fictional characters. Subjects rated the degree of similarity between themselves and these characters. Based on these ratings, for each participant, the fictional characters rated most similar to and most different from oneself served as the protagonists in the imaging session. Then, while being scanned, subjects rated the intensity of emotion resulting from a variety of events happening to themselves (SELF condition) or to one of the two chosen characters (SIMILAR and DISSIMILAR conditions; see Fig. 1). Following scanning, a memory interview was carried out to examine which of the events presented during scanning they actually remembered from their own past experiences.

It was expected that core structures associated with AM such as the hippocampus would show differential activity for events recalled from the past experience of the participant as compared to unrecalled events. It was further predicted that these structures would show increased activation when participants were presented with protagonists similar to themselves than when presented with dissimilar protagonists.

Section snippets

Participants

Twenty individuals (mean age 29, SD = 3.8, 10 women, 3 left-handed), participated in this study. Participants had no reported history of psychiatric or neurological disorders, and were not using psychoactive drugs at the time of the study. In addition, all participants had normal or corrected-to-normal vision. All subjects gave informed consent and were paid for their participation.

Stimuli and procedure

The procedure included three phases: in the pre-scanning phase subjects selected the SIMILAR and the DISSIMILAR

Behavioral results

No significant differences were found in mean of the emotional ratings between the three conditions (SELF, SIMILAR, DISSIMILAR) [F(19,1) = 0.658, p = 0.53, ns].

A correlation analysis (with Bonferroni corrections) between ratings during scanning in the three conditions was conducted to examine whether or not subjects tended to judge a situation in which others were involved similarly to judging events involving themselves, particularly when judging events happening to a similar protagonist. It was

Discussion

While there are conflicting reports regarding the role of AM in mentalizing, here we show that these two processes are related in events subjects recall from their past. The behavioral results demonstrate a strong relationship between emotional judgments of SIMILAR and the SELF but not between DISSIMILAR and SELF suggesting that the subject may have projected internal knowledge on the SIMILAR protagonist. Furthermore, differences were found between the events the subjects recalled vs. events

Conclusions

The results of the present study demonstrate that we not only use our repertoire of memories when judging personal events, but also when judging the emotional state of a similar protagonist. It is possible that the hippocampus serves as a modulator of the empathic response. When another individual experiences an event that one remembers having experienced, it is possible that the hippocampus is recruited during empathy only in cases where subjective similarity to that individual is felt. This

Author contributions

The authors declare no conflict of interest.

Acknowledgments

We would like to thank Dr. Asaf Gilboa for his help in hippocampus tracing and for his comments on the manuscript. We are grateful to Prof. Rachel Tomer for the comments on the manuscript.

This work was supported by the Israeli Scientific Foundation (ISF).

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