Contributions of episodic retrieval and mentalizing to autobiographical thought: evidence from functional neuroimaging, resting-state connectivity, and fMRI meta-analyses

Abstract

A growing number of studies suggest the brain's "default network" becomes engaged when individuals recall their personal past or simulate their future. Recent reports of heterogeneity within the network raise the possibility that these autobiographical processes comprised of multiple component processes, each supported by distinct functional-anatomic subsystems. We previously hypothesized that a medial temporal subsystem contributes to autobiographical memory and future thought by enabling individuals to retrieve prior information and bind this information into a mental scene. Conversely, a dorsal medial subsystem was proposed to support social-reflective aspects of autobiographical thought, allowing individuals to reflect on the mental states of one's self and others (i.e. "mentalizing"). To test these hypotheses, we first examined activity in the default network subsystems as participants performed two commonly employed tasks of episodic retrieval and mentalizing. In a subset of participants, relationships among task-evoked regions were examined at rest, in the absence of an overt task. Finally, large-scale fMRI meta-analyses were conducted to identify brain regions that most strongly predicted the presence of episodic retrieval and mentalizing, and these results were compared to meta-analyses of autobiographical tasks. Across studies, laboratory-based episodic retrieval tasks were preferentially linked to the medial temporal subsystem, while mentalizing tasks were preferentially linked to the dorsal medial subsystem. In turn, autobiographical tasks engaged aspects of both subsystems. These results suggest the default network is a heterogeneous brain system whose subsystems support distinct component processes of autobiographical thought.

Keywords: Autobiographical; Default mode; Default network; Episodic memory; Mentalizing; Self; Social; Theory of mind.

Figure 1. Episodic retrieval and mentalizing preferentially engage medial temporal and dorsal medial subsystems

Exploratory whole-brain analyses were conducted for the episodic retrieval and theory of mind tasks in Part 1, corrected for multiple comparisons, and projected onto a surface template (Van Essen, 2005). A. The episodic memory analysis contrasted Hits-Remember trials with Correct Rejections. B. The mentalizing analysis contrasted False Belief trials with False Photograph trials. C. An overlap analysis reveals common recruitment of the posterior cingulate cortex and distinct recruitment of the default network subsystems. Dotted lines highlight the functional-anatomic boundaries of the default network as defined using resting state clustering techniques by Yeo et al., 2011.

Figure 2. Patterns of task-based functional dissociations are reflected in the brain’s resting state architecture

A. Patterns of resting state functional correlations with a left posterior inferior parietal lobule cluster defined from the episodic memory task in Part 1 are projected onto a surface template (Van Essen, 2005). B. Resting state correlations were also examined with a left temporoparietal junction cluster defined from the mentalizing task. C. The two functional correlation maps in A and B were directly compared by conducting a paired t-test. Note that despite a range of differences within the default network subsystems, minimal differences between the memory-defined and mentalizing-derived parietal seeds were observed in the posterior cingulate cortex and the anterior medial prefrontal cortex – the “hubs” of the default network (marked by an asterisk).

Figure 3. Meta-analyses of episodic retrieval, mentalizing, and autobiographical thought

The Neurosynth framework (Yarkoni et al., 2011) was used to conduct automated meta-analyses of A. episodic recollection tasks, B. mentalizing tasks, and C. autobiographical tasks across a large database of published neuroimaging studies. Shown are whole-brain corrected reverse inference maps reflecting the specificity of the particular pattern of activation for the given task, as compared to a broad corpus of other tasks in the database.

Figure 4. Autobiographical thought comprises multiple component processes

A. In this overlap analysis, whole-brain reverse inference maps from the meta-analyses of episodic retrieval, mentalizing, and autobiographical tasks were corrected for multiple comparisons and overlaid on a surface projection (Van Essen, 2005). B. The association between the top seven functional terms linked to the episodic recollection and mentalizing meta-analyses are shown in relationship to each other (green = episodic recollection; blue = mentalizing) and the autobiographical thought meta-analysis (red). Both panels illustrate the functional differences between episodic recollection and mentalizing and the overlap of both functions with autobiographical memory/future thought. The distance from the origin in the polar plot in Panel B reflects the Pearson correlation across all voxels between each meta-analysis map for the concept as a whole and individual terms in the Neurosynth database. For example, the meta-analysis map for the concept of mentalizing (defined by several related terms) correlated 0.45 with the meta-analysis map for the individual term “social.” If a network map or mask loaded highly on multiple terms that shared a morphological root (e.g., retrieval and retrieved; story and stories), the term with the highest loading was included in the figure.