Behavioral and Brain Sciences An integrative memory model of recollection and familiarity to understand memory deficits cambridge.org/bbs Christine Bastina , Gabriel Bessona, Jessica Simonb, Emma Delhayea, Marie Geurtena, Sylvie Willemsc and Eric Salmona,d Target Article aGIGA-Cyclotron Research Centre In Vivo Imaging & Psychology and Neuroscience of Cognition Research Unit, Cite this article: Bastin C, Besson G, Simon J, University of Liège, 4000 Liège, Belgium; bPsychology and Neuroscience of Cognition Research Unit, University of Delhaye E, Geurten M, Willems S, Salmon E. Liège, 4000 Liège, Belgium; cPsychological and Speech Therapy Consultation Center & Psychology and (2019) An integrative memory model of Neuroscience of Cognition Research Unit, University of Liège, 4000 Liège, Belgium and dMemory Clinic, University recollection and familiarity to understand memory deficits. Behavioral and Brain Sciences Hospital, 4000 Liège, Belgium. 42, e281: 1–60. doi:10.1017/ [email protected] http://www.giga.uliege.be https://www.psyncog.uliege.be S0140525X19000621 [email protected] http://www.giga.uliege.be https://www.psyncog.uliege.be [email protected] https://www.psyncog.uliege.be Target Article Accepted: 22 January 2019 [email protected] http://www.giga.uliege.be https://www.psyncog.uliege.be Target Article Manuscript Online: 5 February [email protected] https://www.psyncog.uliege.be 2019 [email protected] https://www.psyncog.uliege.be Commentaries Accepted: 30 May 2019 [email protected] http://www.giga.uliege.be https://www.psyncog.uliege.be Keywords: Alzheimer’s disease (AD); cerebral network; Abstract dual-process models of recognition memory; episodic memory; familiarity; fluency; Humans can recollect past events in details (recollection) and/or know that an object, per- hippocampus; perirhinal cortex; posterior son, or place has been encountered before (familiarity). During the last two decades, there cingulate cortex; recollection. has been intense debate about how recollection and familiarity are organized in the brain. Here, we propose an integrative memory model which describes the distributed and inter- active neurocognitive architecture of representations and operations underlying recollection What is Open Peer Commentary? What follows on these pages is known as a and familiarity. In this architecture, the subjective experience of recollection and familiarity Treatment, in which a significant and arises from the interaction between core systems (storing particular kinds of representa- controversial Target Article is published tions shaped by specific computational mechanisms) and an attribution system. By inte- along with Commentaries (p. 15) and an grating principles from current theoretical views about memory functioning, we provide Author’s Response (p. 40). See bbsonline. org for more information. a testable framework to refine the prediction of deficient versus preserved mechanisms in memory-impaired populations. The case of Alzheimer’s disease (AD) is considered as an example because it entails progressive lesions starting with limited damage to core sys- tems before invading step-by-step most parts of the model-related network. We suggest a chronological scheme of cognitive impairments along the course of AD, where the inaugu- rating deficit would relate early neurodegeneration of the perirhinal/anterolateral entorhi- nal cortex to impaired familiarity for items that need to be discriminated as viewpoint- invariant conjunctive entities. The integrative memory model can guide future neuropsy- chological and neuroimaging studies aiming to understand how such a network allows humans to remember past events, to project into the future, and possibly also to share experiences. 1. Introduction Episodic memory allows us to remember objects and people that we have encountered as well as details about events that we have personally experienced. It gives us awareness of our past experience, it is crucial to a smooth functioning in our daily life, and it permits that we mentally project what might subsequently happen on the basis of our past memories (Tulving 1999). Unfortunately, episodic memory is fragile and can be disrupted by certain conditions. Some people experience memory impairments (amnesia) suddenly after an acute brain damage. Others experience a progressive memory decline because of a neurodegenerative pathology such as Alzheimer’s disease (AD). The understanding of episodic memory mechanisms and how they are implemented in the brain has progressed extensively thanks to research in neuropsychology and neuroimaging. Current theories posit that episodic memories can be retrieved via two processes: recollection, which designates the recall of the specific details from the initial experience of the events, including details about the spatiotemporal context, and familiarity, which refers to knowing that one has experienced something in the past without recalling details about the encoding © Cambridge University Press 2019 episode (Mandler 1980; Tulving 1985; Yonelinas 1994). In the following sections of this target article, we first define the processes of recollection and familiarity in psychological terms (sect. 2). Then, we summarize the current most influ- ential frameworks that describe their neural substrates. The existing frameworks differ by their focus on cognitive operations versus type of representations, by the emphasis on a Downloaded from https://www.cambridge.org/core. Access paid by the UC San Diego Library, on 03 Jan 2020 at 19:12:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X19000621 2 Bastin et al.: An integrative memory model of recollection and familiarity to understand memory deficits specific brain region versus neural systems, and by the assump- 2. Recollection and familiarity tion that recollection and familiarity processes are either local- In psychological terms, recollection is defined as a retrieval pro- ized to a brain region or not localized (section 2). Next, we cess whereby individuals recall detailed qualitative information consider how a more complete understanding of recollection about studied events (Montaldi & Mayes 2010; Yonelinas et al. and familiarity would benefit from combining different accounts 2010). Some authors consider that there is recollection as soon into a unified framework that bridges several cognitive and neu- as one retrieves at least one detail that is not currently perceived, ral mechanisms (sect. 3). Therefore, we propose an integration inducing moderate to high confidence that the event actually of principles, currently pertaining to separate theories, in a neu- occurred (Higham & Vokey 2004; Yonelinas et al. 2010), but rocognitive architecture of interacting operations and represen- the amount of details may vary from one trial to the other tations within large-scale cerebral networks that allow (Higham & Vokey 2004; Parks & Yonelinas 2007; Wixted & familiarity and recollection (sects. 4 and 5). Such an integrative Mickes 2010). These associated details typically represent the con- perspective allows us to generate new hypotheses about the text in which an event took place (i.e., place, time, environmental nature of memory deficits in brain-lesioned populations and or internal details) (Ranganath 2010). Recollection can be accom- neurodegenerative diseases. Section 6 thus presents predictions panied by a subjective experience of mentally reliving the prior about recollection and familiarity deficits in memory-impaired experience with the event, as if one were mentally traveling populations, with a detailed illustration on AD. back in time to re-experience it (Tulving 1985). In contrast, familiarity is a feeling of oldness indicating that something has been previously experienced. It is thought to support predominantly recognition of single pieces of information (i.e., CHRISTINE BASTIN is assistant professor and research associate of the items such as objects and people; Ranganath 2010), but associations Fonds National de la Recherche Scientifique (FRS-FNRS) at the between similar types of information could also be recognized as University of Liège. She obtained her PhD in psychology in 2004. familiar (Mayes et al. 2007). Subjectively, feelings of familiarity are She has published over 70 scientific articles focusing on cognitive neu- more or less strong feelings that one knows that something has roscience of memory. Her work on early markers of Alzheimer’s dis- already been encountered, leading to varying degrees of confidence ease was awarded the Santkin Prize from the Alzheimer League and the Royal Academy of Medicine of Belgium in 2013. (Tulving 1985; Yonelinas et al. 2010). According to some theories, the feeling of familiarity arises when one interprets enhanced pro- GABRIEL BESSON is a postdoctoral research fellow at the University of cessing fluency of a stimulus as a sign that it was previously encoun- Liège. He received his PhD in neurosciences from the Aix-Marseille tered (Jacoby et al. 1989; Whittlesea et al. 1990). Fluency is typically University in 2013. His research deals with the neural substrates and defined as the speed and ease with which a stimulus is processed and temporal dynamics of memory processes, with a focus on familiar- may arise from many sources (e.g., mere repetition, perceptual clar- ity-based memory. ity, rhyme, predictive context, oral-motor sequence), including past occurrences (Oppenheimer 2008;