Brain Activity and Functional Coupling Changes Associated with Self-Reference Effect during Both Encoding and Retrieval. Nastassja Morel, Nicolas Villain, Géraldine Rauchs, Malo Gaubert, Pascale Piolino, Brigitte Landeau, Florence Mézenge, Béatrice Desgranges, Francis Eustache, Gaël Chételat To cite this version: Nastassja Morel, Nicolas Villain, Géraldine Rauchs, Malo Gaubert, Pascale Piolino, et al.. Brain Activity and Functional Coupling Changes Associated with Self-Reference Effect during Both Encod- ing and Retrieval.. PLoS ONE, Public Library of Science, 2014, 9 (3), pp.e90488. 10.1371/jour- nal.pone.0090488. inserm-00966855 HAL Id: inserm-00966855 https://www.hal.inserm.fr/inserm-00966855 Submitted on 27 Mar 2014 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Brain Activity and Functional Coupling Changes Associated with Self-Reference Effect during Both Encoding and Retrieval Nastassja Morel1,2,3,4, Nicolas Villain1,2,3,4,Ge´raldine Rauchs1,2,3,4, Malo Gaubert1,2,3,4, Pascale Piolino5,6, Brigitte Landeau1,2,3,4, Florence Me´zenge1,2,3,4,Be´atrice Desgranges1,2,3,4, Francis Eustache1,2,3,4, Gae¨lChe´telat1,2,3,4* 1 Inserm, U1077, Caen, France, 2 Universite´ de Caen Basse-Normandie, UMR-S1077, Caen, France, 3 Ecole Pratique des Hautes Etudes, UMR-S1077, Caen, France, 4 CHU de Caen, U1077, Caen, France, 5 Universite´ de Paris Descartes, Laboratoire Me´moire et Cognition, Institut de Psychologie, Paris, France, 6 Inserm, U 894, Centre de Psychiatrie et Neurosciences, Paris, France Abstract Information that is processed with reference to oneself, i.e. Self-Referential Processing (SRP), is generally associated with better remembering compared to information processed in a condition not related to oneself. This positive effect of the self on subsequent memory performance is called as Self-Reference Effect (SRE). The neural basis of SRE is still poorly understood. The main goal of the present work was thus to highlight brain changes associated with SRE in terms of activity and functional coupling and during both encoding and retrieval so as to assess the relative contribution of both processes to SRE. For this purpose, we used an fMRI event-related self-referential paradigm in 30 healthy young subjects and measured brain activity during both encoding and retrieval of self-relevant information compared to a semantic control condition. We found that SRE was associated with brain changes during the encoding phase only, including both greater activity in the medial prefrontal cortex and hippocampus, and greater functional coupling between these brain regions and the posterior cingulate cortex. These findings highlight the contribution of brain regions involved in both SRP and episodic memory and the relevance of the communication between these regions during the encoding process as the neural substrates of SRE. This is consistent with the idea that SRE reflects a positive effect of the reactivation of self-related memories on the encoding of new information in episodic memory. Citation: Morel N, Villain N, Rauchs G, Gaubert M, Piolino P, et al. (2014) Brain Activity and Functional Coupling Changes Associated with Self-Reference Effect during Both Encoding and Retrieval. PLoS ONE 9(3): e90488. doi:10.1371/journal.pone.0090488 Editor: Michelle Hampson, Yale University, United States of America Received August 5, 2013; Accepted January 31, 2014; Published March 7, 2014 Copyright: ß 2014 Morel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Fondation Plan Alzheimer (Alzheimer Plan 2008–2012), Agence Nationale de la Recherche (ANR LONGVIE 2007), Re´gion Basse Normandie, Institut National de la Sante´ et de la Recherche Me´dicale (Inserm) and Ministe`re de l’Enseignement Supe´rieur de la Recherche. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction referential stimuli even if they are differentially involved in the different self-related processes. In addition, the MPFC is One’s sense of self fundamentally depends on self-knowledge considered as a key-component of the Self-Memory System [10] and memories of one’s past experiences [1–3]. The processing of as it is activated regardless of the level of abstraction of information information in a self-referential manner, i.e. with reference to related to the Self (from general self-knowledge to specific oneself, is known as Self-Referential Processing (SRP). SRP autobiographical memories) while other structures would tend to generally consists in linking implicitly or explicitly the information be involved in specific conditions e.g. in relation to the recollection to-be-processed with pre-existent semantic self-knowledge and of autobiographical memories for the hippocampus and the autobiographical memories (for review, [4]). posterior areas [11–14]. Numerous neuroimaging studies have been conducted to assess An extensive literature has demonstrated that SRP enhances the underlying mechanisms of SRP, for example by asking subsequent memory performance. Rogers et al. [15] first reported participants to judge whether a trait adjective describes their that personality trait adjectives rated under a self-reference task personality. These studies consistently reported the involvement of were better recalled than words processed in non self-related cortical midline structures such as the medial prefrontal cortex conditions such as semantic processing. The positive effect of SRP (MPFC) extending to the anterior cingulate cortex (ACC) and the on memory performance is called as Self-Reference Effect (SRE) posterior cingulate cortex (PCC) [5–9]. While other regions are and has been repeatedly observed since then [16–19]. However, also implicated in specific aspects of the self, such as temporo- little is known about the brain correlates of the positive effect of parietal areas in agency (i.e. the feeling of being causally involved SRE. The few previous neuroimaging studies on SRE have in an action), cortical midline structures are thought to be involved consistently reported the involvement of the MPFC, especially the in the ‘‘core self’’ in that they are crucial to the processing of self- ventral MPFC, during either encoding or retrieval [20–23], PLOS ONE | www.plosone.org 1 March 2014 | Volume 9 | Issue 3 | e90488 Neural Basis of Self-Reference Effect on Memory sometimes extending to the anterior cingulate cortex [22] or naming (DO80 [30]). The tests were administered and scored by a together with other brain areas such as the hippocampus [23]. neuropsychologist. No subject complained about his or her These results suggest that SRE may be related to changes mainly memory. Signed informed consent was obtained prior to in cortical midline structures known to be involved in SRP, but participation. The study was approved by the local ethical also in the hippocampus known to be involved in episodic memory committee (CPP Nord-Ouest III) and was carried out in line with processes, during either encoding or retrieval. the declaration of Helsinki. However, no study to date has considered brain activity during both encoding and retrieval. Yet, this is crucial to understand the Data acquisition relative contribution of each process to SRE, i.e to know if Design and task. The fMRI event-related self-referential improved memory performances of self-related information are paradigm used in the present study was adapted from the more related to brain activity changes during the encoding vs the paradigm used in previous publications on SRP and SRE retrieval of this information. More specifically, as previous studies [6,7,31–33]. The selected materials consisted in a list of 204 suggest the involvement of brain structures preferentially involved personality trait adjectives selected from 463 adjectives issued from in self (MPFC), episodic memory (hippocampus), or both processes a French language dictionary (http://atilf.atilf.fr/). The selection (PCC), it seems of particular interest to assess their relative of adjectives was based on their familiarity and valence ratings involvement during encoding versus retrieval of self-related obtained from a pre-experiment in samples of young and elderly information and the role of their interaction in SRE. As SRE is individuals with low and high education. For the sake of the fMRI thought to reflect a positive effect of the reactivation of self-related experiment, 6 lists of 24 adjectives were constituted from the 204 memories on the encoding of new information in episodic memory selected adjectives for the two runs per condition (n = 3) of the [4], we hypothesized that SRE at least partly results from a encoding session and 2 lists of 30 adjectives