Humans can recollect past events in details (recollection) and/or know that an object, person, or place has been encountered before (familiarity). During the last two decades, there 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 interactive neurocognitive architecture of representations and operations underlying recollection and familiarity. In this architecture, the subjective experience of recollection and familiarity arises from the interaction between core systems (storing particular kinds of representations shaped by specific computational mechanisms) and an attribution system. By integrating principles from current theoretical views about memory functioning, we provide 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 systems 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 inaugurating deficit would relate early neurodegeneration of the perirhinal/anterolateral entorhinal cortex to impaired familiarity for items that need to be discriminated as viewpoint-invariant conjunctive entities. The integrative memory model can guide future neuropsychological 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.

The integrative memory model contains multiple subsystems. In this commentary, the processes within these subsystems are questioned. First, the assumption that familiarity largely reflects perceptual fluency is examined. Next, the distinction between “process” and “representational” models of temporal lobe function is challenged. Finally, the “relational representation core system” (or “extended hippocampal system”), which is central to the model, is especially sketchy. Here, I highlight key questions to be addressed in order to understand this system's role in trace formation.

Episodic memories are shaped by the representational format of their contents. These formats are not only determined by medial temporal lobe areas, but essentially also by the neocortical regions which these areas control. The representational formats of medial temporal lobe and neocortex are sufficient to determine both, memory contents and subjective memory qualities, without the further need for an attribution system.

The integrative memory model combines five core memory systems with an attributional system. We agree with Bastin et al. that this melding is the most novel aspect of the model. But we await further evidence that the model's substantial complexity informs our understanding of false memories or of the development of recollection and familiarity.

Although Bastin et al. propose a useful model for thinking about the structure of memory and memory deficits, their distinction between entities and relational encoding is incompatible with data showing that even individual objects – prototypical “entities” – are made up of distinct features which require binding. Thus, “entity” and “relational” brain regions may need to solve fundamentally the same problems.

Despite highlighting the role of the attribution system and proposing a coherent large-scale architecture of declarative memory, the integrative memory model would be more “integrative” if the temporal dynamics of the interactions between its components was clarified. This is necessary to make predictions in patients with brain injury and hypothesize dissociations.

The target article carefully describes the memory system, centered on the temporal lobe that builds specific memory traces. It does not, however, mention the laterality effects that exist within this system. This commentary briefly surveys evidence showing that clear asymmetries exist within the temporal lobe structures subserving the core system and that the right temporal structures mainly underpin face familiarity feelings.

We fully support dissociating the subjective experience from the memory contents in recognition memory, as Bastin et al. posit in the target article. However, having two generic memory modules with qualitatively different functions is not mandatory and is in fact inconsistent with experimental evidence. We propose that quantitative differences in the properties of the memory modules can account for the apparent dissociation of recollection and familiarity along anatomical lines.

We argue that while the proposed memory model by Bastin et al. can explain familiarity-based memory judgements through the interaction of a core representation system and an attribution system, recollection-based memory judgements are not based on non-mnemonic signals being attributed to memory.

Although the integrative memory model proposed by Bastin et al. is interesting, particularly for Alzheimer's disease, it may benefit from incorporating the subjective experience of recollection. We therefore offer complementary lines of interpretation to explain how recollection and familiarity in Alzheimer's disease can be dissociated based not only on accounts of their neural correlates but, critically, on the subjective experience of memory in patients.

Cognitive control constrains retrieval processing and so restricts what comes to mind as input to the attribution system. We review evidence that older adults, patients with Alzheimer's disease, and people with traumatic brain injury exert less cognitive control during retrieval, and so are susceptible to memory misattributions in the form of dramatic levels of false remembering.

Theoretical models of memory retrieval have focused on processes of recollection and familiarity. Research suggests that there are still other processes involved in memory reconstruction, leading to experiences of knowing and inferring the past. Understanding these experiences, and the cognitive processes that give rise to them, seems likely to further expand our understanding of the neural substrates of memory.

We suggest that the inclusion of anxiety, as one relevant mood factor, could enhance the implementation of the integrative memory model in research and the clinic. The role of anxiety in Alzheimer's disease neuroanatomy, symptomology, and progression is used as an example. Customization of the integrative memory model can establish strong foundations for pathology-specific models of memory deficits, enhancing the development of precision medicine applications.

Bastin et al. propose a dual-process model to understand memory deficits. However, results from state-trace analysis have suggested a single underlying variable in behavioral and neural data. We advocate the usage of unidimensional models that are supported by data and have been successful in understanding memory deficits and in linking to neural data.

Misidentification syndromes occur commonly in neuropsychiatric practice and can be explained through aberrant integration of recollection and familiarity, in keeping with a dysfunction at the level of the attributional system in the new integrative memory model. We examine neuroimaging findings associated with Fregoli and Capgras syndromes and compare these with the proposed neural substrate of the integrative memory model supporting the core and attribution functions.

In this commentary on Bastin et al., we suggest that spatial context plays a critical role in the encoding and retrieval of events. Specifically, the translation process between the viewpoint-independent content of a memory and the viewpoint-dependent stimuli activating the retrieval (mental frame syncing) plays a critical role in spatial memory recollection. This perspective also provides an explanatory model for pathological disturbances such as Alzheimer's disease.

According to Bastin et al.’s integrative memory model, familiarity may be attributed to both entity representations and relational representations. However, the model does not specify what triggers familiarity for relational representations. I argue that fluency is a key player in the attribution of familiarity regardless of the type of representation. Two lines of evidence are reviewed in support of my claim.

Bastin et al. present a framework that draws heavily on existing ideas of dual processes in memory in order to make predictions about memory deficits in clinical populations. It has been difficult to find behavioral evidence for multiple memory processes but we offer some evidence for dual processes in a related domain: memory for the time-of-occurrence of events.

The memory impairment of neurological and psychiatric patients is seen as occurring mainly in the autobiographical-episodic memory domain and this is considered to depend on limbic structures such as the amygdala or the septal nuclei. Especially the amygdala is a hub for giving an emotional flavor to personal memories. Bastin et al. fail to include the amygdala in their integrative memory model.

The syndrome of semantic dementia represents the “other side of the coin” to Alzheimer's disease, offering convergent evidence to help refine Bastin et al.’s integrative memory model. By considering the integrative memory model through the lens of semantic dementia, we propose a number of important extensions to the framework, to help clarify the complex neurocognitive mechanisms underlying recollection and familiarity.