Relationships between individual differences in dual process and electrophysiological signatures of familiarity and recollection during retrieval

Our everyday memories can vary in terms of accuracy and phenomenology. One theoretical account that can help understand how to categorize these differences delineates between memories that are remembered versus familiar. This difference largely hinges on whether the memories contain information about both an item itself as well as associated details (Remember) versus those that are devoid of these associated contextual details (Familiar). This distinction has been supported by computational modeling of behavior, studies in patients, and neuroimaging work including differences both in electrophysiological and functional magnetic resonance imaging. Yet, compelling convergent evidence directly linking individual differences in estimates of Recollection and Familiarity, the mathematical estimates of differences in Remember versus Familiar judgments, with their concomitant electrophysiological signatures is lacking. The present study measured memory responses to a recognition memory task while participants underwent simultaneous electrophysiological recordings of brain activity. Non-parametric cluster-based permutation analyses revealed selective associations between electrophysiological signatures ofFamiliarity and Recollection with their respective behavioral estimates. These results support the idea that Recollection and Familiarity are distinct phenomena and is the first to relate individual differences in both Recollection and Familiarity to electrophysiological signatures.

Retrieval Processes

Endel Tulving’s views of synergistic ecphory and cue-dependent forgetting are discussed and endorsed, in particular the view that external stimulation (or self-initiated internal stimulation) necessarily interacts with encoded records to yield retrieval. Paul Kolers’ view of retrieval as repetition of processing operations is also evaluated. Other topics include retrieval as recapitulation of encoding, transfer-appropriate processing, environmental and schematic support, and self-initiated activities. It is concluded that the concepts of levels of processing and transfer-appropriate processing are both necessary to describe observed patterns of retrieval. Two postulated bases for recognition memory—familiarity and recollection—are described and evaluated, as are the ideas of processing fluency and attribution proposed by Larry Jacoby. Finally, studies of involuntary retrieval, mind-wandering, and prospective memory are described and their implications assessed.

Recognition Memory in Noonan Syndrome

Noonan syndrome (NS) and the clinically related NS with multiple lentiginous (NMLS) are genetic conditions characterized by upregulated RAS mitogen activated protein kinase (RAS–MAPK) signaling, which is known to impact hippocampus-dependent memory formation and consolidation. The aim of the present study was to provide a detailed characterization of the recognition memory of children and adolescents with NS/NMLS. We compared 18 children and adolescents affected by NS and NMLS with 22 typically developing (TD) children, matched for chronological age and non-verbal Intelligence Quotient (IQ), in two different experimental paradigms, to assess familiarity and recollection: a Process Dissociation Procedure (PDP) and a Task Dissociation Procedure (TDP). Differences in verbal skills between groups, as well as chronological age, were considered in the analysis. Participants with NS and NSML showed reduced recollection in the PDP and impaired associative recognition in the TDP, compared to controls. These results indicate poor recollection in the recognition memory of participants with NS and NSML, which cannot be explained by intellectual disability or language deficits. These results provide evidence of the role of mutations impacting RAS–MAPK signaling in the disruption of hippocampal memory formation and consolidation.

Encoding-linked pupil response is modulated by expected and unexpected novelty: Implications for memory formation and neurotransmission

Whether a novel stimulus is expected or unexpected may have implications for the kind of ensuing encoding and the type of subsequent memory. Pupil response was used in the present study to explore the way expected and unexpected stimuli are encoded and whether encoding-linked pupil response is modulated by expectation. Participants first established a contingency relationship between a series of symbols and the type of stimulus (man-made or natural) that followed each one. At encoding, some of the target stimuli violated the previously established relationship (i.e., unexpected), while the majority conformed to this relationship (i.e., expected). Expectation at encoding had opposite effects on familiarity and recollection, the two types of memory that support recognition, and modulated differently the way pupil responses predicted subsequent memory. Encoding of unexpected novel stimuli was associated with increased pupil dilation as a predictor of subsequent memory type and strength. In contrast, encoding of expected novel stimuli was associated with decreased pupil response (constriction), which was predictive of subsequent memory type and strength. The findings support the close link between pupil response and memory formation, but critically indicate that this is modulated by the type of novelty as defined by expectation. These novel findings have important implications for the encoding mechanisms involved when different types of novelty are detected and is proposed to indicate the operation of different neurotransmitters in memory formation.

Disturbed temporal dynamics of episodic retrieval activity with preserved spatial activity pattern in amnestic mild cognitive impairment: A simultaneous EEG-fMRI study

Background Episodic memory (EM) deficit is the core cognitive dysfunction of amnestic mild cognitive impairment (aMCI). However, the episodic retrieval circuit detected by functional MRI (fMRI) appears preserved in aMCI subjects. To address this discrepancy, this study employed simultaneous electroencephalography (EEG)-fMRI recording to determine whether temporal dynamics of brain episodic retrieval activity were disturbed in patients with aMCI. Methods Twenty-six aMCI and 29 healthy control (HC) subjects completed a word-list memory retrieval task during simultaneous EEG-fMRI. The retrieval success activation pattern was detected with fMRI analysis, and the familiarity- and recollection-related components of episodic retrieval activity were identified using event-related potential (ERP) analysis. The fMRI-constrained ERP analysis explored the temporal dynamics of brain activity in the retrieval success pattern, and the ERP-informed fMRI analysis detected fMRI correlates of the ERP components related to familiarity and recollection processes. Results The two groups exhibited similar retrieval success patterns in the bilateral posteromedial parietal cortex, the left inferior parietal lobule (IPL), and the left lateral prefrontal cortex (LPFC). The fMRI-constrained ERP analysis showed that the aMCI group did not exhibit old/new effects in the IPL and LPFC that were observed in the HC group. In addition, the aMCI group showed decreased fMRI activity in the precuneus and left hippocampus related to ERP familiarity and recollection components, respectively. Conclusions This study identified disturbed temporal dynamics in episodic retrieval activity with a preserved spatial activity pattern in aMCI. Taken together, the simultaneous EEG-fMRI technique demonstrated the potential to identify individuals with a high risk of cognitive deterioration.

Thalamic-Medial Temporal Lobe Connectivity Underpins Familiarity Memory

The neural basis of memory is highly distributed, but the thalamus is known to play a particularly critical role. However, exactly how the different thalamic nuclei contribute to different kinds of memory is unclear. Moreover, whether thalamic connectivity with the medial temporal lobe (MTL), arguably the most fundamental memory structure, is critical for memory remains unknown. We explore these questions using an fMRI recognition memory paradigm that taps familiarity and recollection (i.e., the two types of memory that support recognition) for objects, faces, and scenes. We show that the mediodorsal thalamus (MDt) plays a material-general role in familiarity, while the anterior thalamus plays a material-general role in recollection. Material-specific regions were found for scene familiarity (ventral posteromedial and pulvinar thalamic nuclei) and face familiarity (left ventrolateral thalamus). Critically, increased functional connectivity between the MDt and the parahippocampal (PHC) and perirhinal cortices (PRC) of the MTL underpinned increases in reported familiarity confidence. These findings suggest that familiarity signals are generated through the dynamic interaction of functionally connected MTL-thalamic structures.

Dissociation of dorso-lateral and dorso-medial prefrontal cortex contributions to familiarity and recollective processes in primates

According to dual-process theories, recognition memory draws upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to familiarity and recollection processes but frequency-specific neuronal activities are considered to play a key role. Here, non-human primate (NHP) electrophysiological local field potential (LFP) recordings first showed that a specific subregion of macaque PFC (i.e., dorsolateral PFC, dlPFC) was implicated in task performance at a specific frequency (i.e., increased beta power in the 10-15 Hz range observed in correct versus error trials) in a specific phase of a recognition memory task (i.e., during sample presentation). Then, to assess generalization to humans and causality we targeted left human dlPFC (BA 9/46) as well as left dorsomedial prefrontal cortex (BA 8/9) for comparison, and also vertex as a control, with transcranial magnetic stimulation at a frequency in the middle of the low-beta range observed in NHP (i.e. 12.5 Hz) and compared that to non-frequency-specific stimulation, and also to a no-stimulation control, during occasional sample presentations within a similar task. Hence we investigated hypotheses about the causal importance for human memory of a location-specific, frequency-specific, and task-epoch-specific intervention derived directly from the NHP electrophysiological observations. Using a dual-process signal detection (DPSD) model based on analysing receiver operating characteristics (ROC) curves, we showed beta-frequency TMS caused decreased recollection when targeted to human dlPFC, but enhanced familiarity when targeted to dorsomedial prefrontal cortex. Non-frequency-specific patterns of stimulation to all sites, and beta-frequency stimulation to vertex, were all without behavioural effect. This study provides causal evidence that PFC-mediated contributions to object recognition memory are modulated by beta-frequency activity; more broadly it provides translational evidence bridging NHPs and humans by emphasizing functional roles of beta-frequency activity in homologous brain regions in recognition memory.Highlightslow beta power in NHP dlPFC during stimulus encoding was related to behaviourhuman rTMS study used parameters derived from NHP observations to test causalitylow beta rTMS to human dlPFC, but not dmPFC, impairs recollectionlow beta rTMS to human dmPFC, but not dlPFC, enhances familiarityprovides cross-species validation of prefrontal beta power to primate recognition

Similar time course of fast familiarity and slow recollection processes for recognition memory in humans and macaques

According to dual-process theory, recognition memory performance draws upon two processes, familiarity and recollection. The relative contribution to recognition memory are commonly distinguished in humans by analyzing receiver-operating-characteristics (ROC) curves; analogous methods are more complex and very rare in animals but fast familiarity and slow recollective-like processes (FF/SR) have been detected in non-human primates (NHPs) based on analyzing recognition error response time profiles. The relative utility of these methods to investigate familiarity and recollection/recollection-like processes across species is uncertain; indeed, even how comparable the FF/SR measures are across humans and NHPs remains unclear. Therefore in this study a broadly similar recognition memory task was exploited in both humans and NHPs to investigate the time course of the two recognition processes. We first show that the FF/SR dissociation exists in this task in human participants and then we demonstrate a similar profile in NHPs which suggests that FF/SR processes are comparable across species. We then verified, using ROC-derived indices for each time-bin in the FF/SR profile, that the ROC and FF/DR measures are related. Hence we argue that the FF/SR approach, procedurally easier in animals, can be used as a decent proxy to investigate these two recognition processes in future animal studies, important given that scant data exists as to the neural basis underlying recollection yet many of the most informative techniques primarily exist in animal models.

Investigating the Influence of the Brain-Derived Neurotrophic Factor Val66Met Single Nucleotide Polymorphism on Familiarity and Recollection Event-Related Potentials

The Val66Met single nucleotide polymorphism (SNP) has previously been reported to impact performance on recognition memory tasks. Whether the two subprocesses of recognition—familiarity and recollection—are differentially impacted by the Val66Met SNP remains unknown. Using event-related potentials (ERPs) recorded during a source memory task, we attempted to dissociate these two subprocesses. Behaviourally, we used participants’ scores on an item-recognition subtask as a measure of familiarity, and participants’ scores on a source-recognition subtask as a measure of recollection. Our findings reveal that Val/Val individuals outperform Met allele carriers on the item-but not the source-recognition task. Electrophysiologically, we were interested in the N400, an early frontal component previously linked to familiarity, and the late positive complex (LPC), a posterior component linked to recollection. We found evidence for Val/Val individuals having larger amplitudes of the LPC compared to Met allele carriers, and evidence for no difference in the N400 amplitudes of these groups. Based on the lack of dissociation between familiarity- and recollection-specific ERPs at the LPC time window, we argue that our behavioural and ERP results might reflect better item-recognition for Val/Val individuals compared to Met allele carriers. We further suggest that both these results reflect differences related to familiarity, rather than recollection.