Remembering objects

Conscious recollection, of the kind characterised by sensory mental imagery, is often thought to involve ‘episodically’ recalling experienced events in one’s personal past. One might wonder whether this overlooks distinctive ways in which we sometimes recall ordinary, persisting objects. Of course, one can recall an object by remembering an event in which one encountered it. But are there acts of recall which are distinctively objectual in that they are not about objects in this mediated way (i.e., by way of being about events in which they featured)? This question has broad implications, not least for understanding the nature and role of imagery in remembering, the requirements of memory-based singular thought about objects, and the sense in which remembering involves ‘mental time travel’ through which one ‘relives’ past events. In this paper, I argue that we sometimes do recall objects from our past without remembering events in which they featured. The positive view of such cases I go on to propose draws on a wide body of empirical work in its support and accommodates a more nuanced picture of the role of imagery in remembering. Succinctly, remembering might essentially involve a kind of ‘re-experiencing’, but it need not involve ‘reliving’.

The spatial distribution of attention predicts familiarity strength during encoding and retrieval

The memories we form are determined by what we attend to, and conversely, what we attend to is influenced by our memory for past experiences. Although we know that shifts of attention via eye movements are related to memory during encoding and retrieval, the role of specific memory processes in this relationship is unclear. There is evidence that attention may be especially important for some forms of memory (i.e., conscious recollection), and less so for others (i.e., familiarity-based recognition and unconscious influences of memory), but results are conflicting with respect to both the memory processes and eye movement patterns involved. To address this, we used a confidence-based method of isolating eye movement indices of spatial attention that are related to different memory processes (i.e., recollection, familiarity strength, and unconscious memory) during encoding and retrieval of real-world scenes. We also developed a new method of measuring the dispersion of eye movements, which proved to be more sensitive to memory processing than previously used measures. Specifically, in two studies, we found that familiarity strength—that is, changes in subjective reports of memory confidence—increased with i) more dispersed patterns of viewing during encoding, ii) less dispersed viewing during retrieval, and iii) greater overlap in regions viewed between encoding and retrieval (i.e., resampling). Recollection was also related to these eye movements in a similar manner, though the associations with recollection were less consistent across experiments. Furthermore, we found no evidence for effects related to unconscious influences of memory. These findings indicate that attentional processes during viewing may not preferentially relate to recollection, and that the spatial distribution of eye movements is directly related to familiarity-based memory during encoding and retrieval.

Posterior hippocampal spindle-ripples co-occur with neocortical theta-bursts and down-upstates, and phase-lock with parietal spindles during NREM sleep in humans

Human anterior and posterior hippocampus (aHC, pHC) differ in connectivity and behavioral correlates. Here we report physiological differences. During NREM sleep, the human hippocampus generates sharpwave-ripples (SWR) similar to those which in rodents mark memory replay. We show that while pHC generates SWR, it also generates about as many spindle-ripples (SSR: ripples phase-locked to local spindles). In contrast, SSR are rare in aHC. Like SWR, SSR often co-occur with neocortical theta bursts (TB), downstates (DS), spindles (SS) and upstates (US), which coordinate cortico-hippocampal interactions and facilitate consolidation in rodents. SWR co-occur with these waves in widespread cortical areas, especially fronto-central. These waves typically occur in the sequence TB-DS-SS-US, with SWR usually occurring prior to SS-US. In contrast, SSR occur ∼350 ms later, with a strong preference for co-occurrence with posterior-parietal SS. pHC-SS were strongly phase-locked with parietal-SS, and pHC-SSR were phase-coupled with pHC-SS and parietal-SS. Human SWR (and associated replay events, if any) are separated by ∼5 s on average, whereas ripples on successive SSR peaks are separated by only ∼80 ms. These distinctive physiological properties of pHC-SSR enable an alternative mechanism for hippocampal engagement with neocortex.Significance StatementRodent hippocampal neurons replay waking events during sharpwave-ripples in NREM sleep, facilitating memory transfer to a permanent cortical store. We show that human anterior hippocampus also produces sharpwave-ripples, but spindle-ripples predominate in posterior. Whereas sharpwave-ripples typically occur as cortex emerges from inactivity, spindle-ripples typically occur at peak cortical activity. Furthermore, posterior hippocampal spindle-ripples are tightly coupled to posterior parietal locations activated by conscious recollection. Finally, multiple spindle-ripples can recur within a second, whereas sharpwave-ripples are separated by about 5s. The human posterior hippocampus is considered homologous to rodent dorsal hippocampus, which is thought to be specialized for consolidation of specific memory details. We speculate that these distinct physiological characteristics of posterior hippocampal spindle-ripples may support a related function in humans.

Conscious and unconscious memory differentially impact attention: Eye movements, visual search, and recognition processes

A hotly debated question is whether memory influences attention through conscious or unconscious processes. To address this controversy, we measured eye movements while participants searched repeated real-world scenes for embedded targets, and we assessed memory for each scene using confidence-based methods to isolate different states of subjective memory awareness. We found that memory-informed eye movements during visual search were predicted both by conscious recollection, which led to a highly precise first eye movement toward the remembered location, and by unconscious memory, which increased search efficiency by gradually directing the eyes toward the target throughout the search trial. In contrast, these eye movement measures were not influenced by familiarity-based memory (i.e., changes in subjective reports of memory strength). The results indicate that conscious recollection and unconscious memory can each play distinct and complementary roles in guiding attention to facilitate efficient extraction of visual information.

Egocentric coding of external items in the lateral entorhinal cortex

Episodic memory, the conscious recollection of past events, is typically experienced from a first-person (egocentric) perspective. The hippocampus plays an essential role in episodic memory and spatial cognition. Although the allocentric nature of hippocampal spatial coding is well understood, little is known about whether the hippocampus receives egocentric information about external items. We recorded in rats the activity of single neurons from the lateral entorhinal cortex (LEC) and medial entorhinal cortex (MEC), the two major inputs to the hippocampus. Many LEC neurons showed tuning for egocentric bearing of external items, whereas MEC cells tended to represent allocentric bearing. These results demonstrate a fundamental dissociation between the reference frames of LEC and MEC neural representations.

Late Positive Component Event-related Potential Amplitude Predicts Long-term Classroom-based Learning

It is difficult to predict whether newly learned information will be retrievable in the future. A biomarker of long-lasting learning, capable of predicting an individual's future ability to retrieve a particular memory, could positively influence teaching and educational methods. ERPs were investigated as a potential biomarker of long-lasting learning. Prior ERP studies have supported a dual-process model of recognition memory that categorizes recollection and familiarity as distinct memorial processes with distinct ERP correlates. The late positive component is thought to underlie conscious recollection and the frontal N400 signal is thought to reflect familiarity [Yonelinas, A. P. Components of episodic memory: The contribution of recollection and familiarity. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 356, 1363–1374, 2001]. Here we show that the magnitude of the late positive component, soon after initial learning, is predictive of subsequent recollection of anatomical terms among medical students 6 months later.

Virtual Reality for Assessment of Episodic Memory in Normal and Pathological Aging

Memory is one of the most important cognitive functions in a person’s life. Memory is essential for recalling personal memories and for performing many everyday tasks, such as reading, playing music, returning home, and planning future actions, and, more generally, memory is crucial for interacting with the world. Determining how humans encode, store, and retrieve memories has a long scientific history, beginning with the classical research by Ebbinghaus in the late 20th century (Ebbinghaus, 1964). Since this seminal work, the large number of papers published in the domain of memory testifies that understanding memory is one of the most important challenges in cognitive neurosciences. With population growth and population aging, understanding memory failures both in the healthy elderly and in neurological and psychiatric conditions is a major societal issue. A substantial body of evidence, mainly from double dissociations observed in neuropsychological patients, has led researchers to consider memory not as a unique entity but as comprising several forms with distinct neuroanatomical substrates (Squire, 2004). With reference to long-term memory, episodic memory may be described as the conscious recollection of personal events combined with their phenomenological and spatiotemporal encoding contexts, such as recollecting one’s wedding day with all the contextual details (Tulving, 2002). Episodic memory is typically opposed to semantic memory, which is viewed as a system dedicated to the storage of facts and general decontextualized knowledge (e.g., Paris is the capital of France), including also the mental lexicon. Episodic memory was initially defined by Tulving as a memory system specialized in storing specific experiences in terms of what happened and where and when it happened (Tulving, 1972). Later, phenomenological processes were associated with the retrieval of memories (Tulving, 2002). Episodic memory is assumed to depend on the self, and involves mental time travel and a sense of reliving the original encoding context that includes autonoetic awareness (i.e., the awareness that this experience happened to oneself, is not happening now, and is part of one’s personal history).

Unintentional and Intentional Recognition Rely on Dissociable Neurocognitive Mechanisms

Distractibility can lead to accidents and academic failures as well as memory problems. Recent evidence suggests that intentional recognition memory can be biased by unintentional recognition of distracting stimuli in the same environment. It is unknown whether unintentional and intentional recognition depend on the same underlying neurocognitive mechanisms. We assessed whether human participants' recognition of previously seen (old) or not seen (new) target stimuli was affected by whether a to-be-ignored distractor was old or new. ERPs were recorded to investigate the neural correlates of this bias. The results showed that the old/new status of salient distractors had a biasing effect on target recognition accuracy. Both intentional and unintentional recognition elicited early ERP effects that are thought to reflect relatively automatic memory processes. However, only intentional recognition elicited the later ERP marker of conscious recollection, consistent with previous suggestions that recollection is under voluntary control. In contrast, unintentional recognition was associated with an enhanced late posterior negativity, which may reflect monitoring or evaluation of memory signals. The findings suggest that unintentional and intentional recognition involve dissociable memory processes.