Differential Contributions of Default and Dorsal Attention Networks to Remembering Thoughts and External Stimuli From Real-Life Events

Cerebral Cortex, November 2018;28: 4023–4035 doi: 10.1093/cercor/bhx270 Advance Access Publication Date: 17 October 2017 Original Article ORIGINAL ARTICLE and External Stimuli From Real-Life Events David Stawarczyk1, Olivier Jeunehomme1 and Arnaud D’Argembeau1,2 1 Department of Psychology, Psychology and Neuroscience of Cognition Research Unit, University of Liège, 4000 Liège, Belgium and 2GIGA-CRC In Vivo Imaging, University of Liège, 4000 Liège, Belgium Address correspondence to David Stawarczyk, Department of Psychology, University of Liège, Quartier Agora, Place des Orateurs 1, 4000 Liège 1, Belgium. E-mail: Abstract Episodic memories are typically composed of perceptual information derived from the external environment and representations of internal states (e.g., one’s thoughts during prior episodes). To date, however, research has mostly focused on the remembrance of external stimuli, such that little is known about how internal mentation is represented within episodic memory. In the present fMRI study, we examined the neural correlates of these 2 components of episodic memories using a novel method of cuing memories from photographs taken during real-life events. We found that, compared with corresponding semantic memory tasks, memories for internal thoughts and external elements were associated with activity in brain areas supporting episodic recollection. Most importantly, however, the 2 kinds of memories also showed differential activation in large-scale brain networks: the remembrance of external elements was associated with greater activity in the dorsal attention network, whereas memories of internal thoughts mainly recruited default network areas. These findings shed new light on the representation of internal and external aspects of prior experience within episodic memory. The default network may contribute to the reinstatement of thoughts experienced during past events, whereas the dorsal attention network may support the allocation of attention to visuospatial features within episodic memory representations. Key words: episodic memory, functional neuroimaging, scene construction, self-generated thought, visuospatial processing Historically, research on episodic memory has mostly focused on the remembrance of stimuli from the external environment, such as lists of words or pictures (Baddeley et al. 2002; Tulving 2002). However, recent advances in the study of human cognition have shown that we spend a substantial amount of time and resources generating thoughts and images that are decoupled from sensory input (Andrews-Hanna, Smallwood, et al. 2014; Smallwood and Schooler 2015; Christoff et al. 2016), which may play important roles in planning, decision making, mood regulation, and creativity (Andrews-Hanna 2012; Beaty et al. 2016). Being able to remember one’s own thoughts and ideas (e.g., possible solutions to daily life issues, evaluations of recently introduced individuals, personal interpretations of events) may critically contribute to adaptive cognitive and social functioning, yet little is currently known about memory for internal mentation. Most notably, commonalities and differences in the cognitive and neural mechanisms underlying the retrieval of inner thoughts versus stimuli from the external environment remain to be investigated in detail. Memory for thoughts has been previously investigated in the context of reality monitoring judgments (i.e., as a means to determine whether a past event was real or imagined; Johnson 1988a; Horton et al. 2007), but it has rarely been a topic of study in itself (but see Brewer 1988; Muhlert et al. 2010). Neuroimaging © The Author 2017. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: Differential Contributions of Default and Dorsal Attention Networks to Remembering Thoughts 4024 | Cerebral Cortex, 2018, Vol. 28, No. 11 that allowed us to investigate commonalities and differences in the processing of perceptual versus reflective information in episodic and semantic memory. We were particularly interested in examining the respective contribution of the default, dorsal attention, and frontoparietal control networks to the retrieval of internal thoughts and external elements from episodic memory. As noted above, the DN is consistently involved in remembering real-life events and research has shown that it comprises at least 2 subsystems that converge on 2 hub-like core regions—the posterior cingulate cortex and anterior medial prefrontal cortex (AndrewsHanna et al. 2010; Andrews-Hanna, Smallwood, et al. 2014). The first subsystem is anchored in the dorsal part of the medial prefrontal cortex and is thought to play an important role in introspecting about mental states and in processing abstract (compared with perceptual) information (Wang et al. 2010, 2013; Christoff et al. 2016), whereas the second subsystem involves the medial temporal lobe and supports the retrieval and binding of episodic elements (Andrews-Hanna 2012; Andrews-Hanna, Saxe, et al. 2014). Based on this fractionation of the DN and previous studies of reality monitoring (Simons et al. 2017), we predicted that the retrieval of internal and external aspects of past events would both rely on DN regions but that memories for internal thoughts would recruit the medial prefrontal cortex and other regions of the dorsal medial subsystem (such as the lateral temporal cortex; AndrewsHanna, Smallwood, et al. 2014) to a greater extent than memories for external elements. The second network of interest in this study was the dorsal attention network (DAN), which supports the top-down control of visuospatial attention and thus plays an important role in processing stimuli from the external environment (Corbetta and Shulman 2002; Spreng et al. 2013). The DN and DAN often show anticorrelated activity, which has led to the view that they support opposite or competitive functions respectively corresponding to the processing of internal versus external information (Fox et al. 2005; Sestieri et al. 2010). However, this view has been challenged by recent studies showing that the DAN can be transiently activated during memory retrieval (in the absence of external cues), and shows an increased functional connectivity with the core midline regions of the DN in this condition (Kragel and Polyn 2015; see also Dixon et al. 2017). While this research reveals a role of the DAN in episodic memory retrieval, its precise function remains unclear. Here, we investigated the possibility that the DAN may not only support the processing of stimuli from the immediate external environment (Corbetta and Shulman 2002), but may also play a role in processing internally generated information referring to aspects of the external world, such as the sensory-perceptual components of episodic memories. Support for this proposal comes from a source memory study showing that remembering prior perceptual versus conceptual judgements about (...truncated)