Eye movements reinstate remembered locations during episodic simulation.

Imagining the future, like recalling the past, relies on the ability to retrieve and imagine a spatial context. Research suggests that eye movements support this process by reactivating spatial contextual details from memory, a process termed gaze reinstatement. While gaze reinstatement has been linked to successful memory retrieval, it remains unclear whether it supports the related process of future simulation. In the present study, we recorded both eye movements and audio while participants described familiar locations from memory and subsequently imagined future events occurring in those locations while either freely moving their eyes or maintaining central fixation. Restricting viewing during simulation significantly reduced self-reported vividness ratings, supporting a critical role for eye movements in simulation. When viewing was unrestricted, participants spontaneously reinstated gaze patterns specific to the simulated location, replicating findings of gaze reinstatement during memory retrieval. Finally, gaze-based location reinstatement was predictive of simulation success, indexed by the number of internal (episodic) details produced, with both measures peaking early and co-varying over time. Together, these findings suggest that the same oculomotor processes that support episodic memory retrieval - that is, gaze-based reinstatement of spatial context - also support episodic simulation.

Peering into the future: Eye movements predict neural repetition effects during episodic simulation.

Imagining future scenarios involves recombining different elements of past experiences into a coherent event, a process broadly supported by the brain's default network. Prior work suggests that distinct brain regions may contribute to the inclusion of different simulation features. Here we examine how activity in these brain regions relates to the vividness of future simulations. Thirty-four healthy young adults imagined future events with familiar people and locations in a two-part study involving a repetition suppression paradigm. First, participants imagined events while their eyes were tracked during a behavioral session. Immediately after, participants imagined events during MRI scanning. The events to be imagined were manipulated such that some were identical to those imagined in the behavioral session while others involved new locations, new people, or both. In this way, we could examine how self-report ratings and eye movements predict brain activity during simulation along with specific simulation features. Vividness ratings were negatively correlated with eye movements, in contrast to an often-observed positive relationship with past recollection. Moreover, fewer eye movements predicted greater involvement of the hippocampus during simulation, an effect specific to location features. Our findings suggest that eye movements may facilitate scene construction for future thinking, lending support to frameworks that spatial information forms the foundation of episodic simulation.

Schema-related eye movements support episodic simulation.

Recent work indicates that eye movements support the retrieval of episodic memories by reactivating the spatiotemporal context in which they were encoded. Although similar mechanisms have been thought to support simulation of future episodes, there is currently no evidence favoring this proposal. In the present study, we investigated the role of eye movements in episodic simulation by comparing the gaze patterns of individual participants imagining future scene and event scenarios to across-participant gaze templates for those same scenarios, reflecting their shared features (i.e., schemas). Our results provide novel evidence that eye movements during episodic simulation in the face of distracting visual noise are (1) schema-specific and (2) predictive of simulation success. Together, these findings suggest that eye movements support episodic simulation via reinstatement of scene and event schemas, and more broadly, that interactions between the memory and oculomotor effector systems may underlie critical cognitive processes including constructive episodic simulation.

Cluttered memory representations shape cognition in old age.

Declines in episodic memory in older adults are typically attributed to differences in encoding strategies and/or retrieval processes. These views omit a critical factor in age-related memory differences: the nature of the representations that are formed. Here, we review evidence that older adults create more cluttered (or richer) representations of events than do younger adults. These cluttered representations might include target information along with recently activated but no-longer-relevant information, prior knowledge cued by the ongoing situation, as well as irrelevant information in the current environment. Although these representations can interfere with the retrieval of target information, they can also support other memory-dependent cognitive functions.

Neural Correlates of Subsequent Memory-Related Gaze Reinstatement.

Mounting evidence linking gaze reinstatement-the recapitulation of encoding-related gaze patterns during retrieval-to behavioral measures of memory suggests that eye movements play an important role in mnemonic processing. Yet, the nature of the gaze scanpath, including its informational content and neural correlates, has remained in question. In this study, we examined eye movement and neural data from a recognition memory task to further elucidate the behavioral and neural bases of functional gaze reinstatement. Consistent with previous work, gaze reinstatement during retrieval of freely viewed scene images was greater than chance and predictive of recognition memory performance. Gaze reinstatement was also associated with viewing of informationally salient image regions at encoding, suggesting that scanpaths may encode and contain high-level scene content. At the brain level, gaze reinstatement was predicted by encoding-related activity in the occipital pole and BG, neural regions associated with visual processing and oculomotor control. Finally, cross-voxel brain pattern similarity analysis revealed overlapping subsequent memory and subsequent gaze reinstatement modulation effects in the parahippocampal place area and hippocampus, in addition to the occipital pole and BG. Together, these findings suggest that encoding-related activity in brain regions associated with scene processing, oculomotor control, and memory supports the formation, and subsequent recapitulation, of functional scanpaths. More broadly, these findings lend support to Scanpath Theory's assertion that eye movements both encode, and are themselves embedded in, mnemonic representations.

Aging changes the interactions between the oculomotor and memory systems.

The use of multi-modal approaches, particularly in conjunction with multivariate analytic techniques, can enrich models of cognition, brain function, and how they change with age. Recently, multivariate approaches have been applied to the study of eye movements in a manner akin to that of neural activity (i.e., pattern similarity). Here, we review the literature regarding multi-modal and/or multivariate approaches, with specific reference to the use of eyetracking to characterize age-related changes in memory. By applying multi-modal and multivariate approaches to the study of aging, research has shown that aging is characterized by moment-to-moment alterations in the amount and pattern of visual exploration, and by extension, alterations in the activity and function of the hippocampus and broader medial temporal lobe (MTL). These methodological advances suggest that age-related declines in the integrity of the memory system has consequences for oculomotor behavior in the moment, in a reciprocal fashion. Age-related changes in hippocampal and MTL structure and function may lead to an increase in, and change in the patterns of, visual exploration in an effort to upregulate the encoding of information. However, such visual exploration patterns may be non-optimal and actually reduce the amount and/or type of incoming information that is bound into a lasting memory representation. This research indicates that age-related cognitive impairments are considerably broader in scope than previously realized.

Encoding and retrieval eye movements mediate age differences in pattern completion.

Older adults often mistake new information as 'old', yet the mechanisms underlying this response bias remain unclear. Typically, false alarms by older adults are thought to reflect pattern completion - the retrieval of a previously encoded stimulus in response to partial input. However, other work suggests that age-related retrieval errors can be accounted for by deficient encoding processes. In the present study, we used eye movement monitoring to quantify age-related changes in behavioral pattern completion as a function of eye movements during both encoding and partially cued retrieval. Consistent with an age-related encoding deficit, older adults executed more gaze fixations and more similar eye movements across repeated image presentations than younger adults, and such effects were predictive of subsequent recognition memory. Analysis of eye movements at retrieval further indicated that in response to partial lure cues, older adults reactivated the similar studied image, indexed by the similarity between encoding and retrieval gaze patterns, and did so more than younger adults. Critically, reactivation of encoded image content via eye movements was associated with lure false alarms in older adults, providing direct evidence for a pattern completion bias. Together, these findings suggest that age-related changes in both encoding and retrieval processes, indexed by eye movements, underlie older adults' increased vulnerability to memory errors.

How Older Adults Remember the World Depends On How They See It.

Age-related changes in visual exploration and memory have typically been studied separately. However, recent evidence suggests that mnemonic processes both affect, and are affected by, eye movements (EMs). Thus, by relating older adults' memory deficits to age-specific visual exploration patterns, we can improve upon models of cognitive aging.

Eye movements support behavioral pattern completion.

The ability to recall a detailed event from a simple reminder is supported by pattern completion, a cognitive operation performed by the hippocampus wherein existing mnemonic representations are retrieved from incomplete input. In behavioral studies, pattern completion is often inferred through the false endorsement of lure (i.e., similar) items as old. However, evidence that such a response is due to the specific retrieval of a similar, previously encoded item is severely lacking. We used eye movement (EM) monitoring during a partial-cue recognition memory task to index reinstatement of lure images behaviorally via the recapitulation of encoding-related EMs or gaze reinstatement. Participants reinstated encoding-related EMs following degraded retrieval cues and this reinstatement was negatively correlated with accuracy for lure images, suggesting that retrieval of existing representations (i.e., pattern completion) underlies lure false alarms. Our findings provide evidence linking gaze reinstatement and pattern completion and advance a functional role for EMs in memory retrieval.

Effects of prior knowledge on active vision and memory in younger and older adults.

In our daily lives we rely on prior knowledge to make predictions about the world around us such as where to search for and locate common objects. Yet, equally important in visual search is the ability to inhibit such processes when those predictions fail. Mounting evidence suggests that relative to younger adults, older adults have difficulty retrieving episodic memories and inhibiting prior knowledge, even when that knowledge is detrimental to the task at hand. However, the consequences of these age-related changes for visual search remain unclear. In the present study, we used eye movement monitoring to investigate whether overreliance on prior knowledge alters the gaze patterns and performance of older adults during visual search. Younger and older adults searched for target objects in congruent or incongruent locations in real-world scenes. As predicted, targets in congruent locations were detected faster than targets in incongruent locations, and this effect was enhanced in older adults. Analysis of viewing behavior revealed that prior knowledge effects emerged early in search, as evidenced by initial saccades, and continued throughout search, with greater viewing of congruent regions by older relative to younger adults, suggesting that schema biasing of online processing increases with age. Finally, both younger and older adults showed enhanced memory for the location of congruent targets and the identity of incongruent targets, with schema-guided viewing during search predicting poor memory for schema-incongruent targets in younger adults on both tasks. Our results provide novel evidence that older adults' overreliance on prior knowledge has consequences for both active vision and memory. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Eye Movements Actively Reinstate Spatiotemporal Mnemonic Content.

Eye movements support memory encoding by binding distinct elements of the visual world into coherent representations. However, the role of eye movements in memory retrieval is less clear. We propose that eye movements play a functional role in retrieval by reinstating the encoding context. By overtly shifting attention in a manner that broadly recapitulates the spatial locations and temporal order of encoded content, eye movements facilitate access to, and reactivation of, associated details. Such mnemonic gaze reinstatement may be obligatorily recruited when task demands exceed cognitive resources, as is often observed in older adults. We review research linking gaze reinstatement to retrieval, describe the neural integration between the oculomotor and memory systems, and discuss implications for models of oculomotor control, memory, and aging.

Fixation reinstatement supports visuospatial memory in older adults.

Research using eye movement monitoring suggests that recapitulating the pattern of eye movements made during stimulus encoding at subsequent retrieval supports memory by reinstating the spatial layout of the encoded stimulus. In the present study, the authors investigated whether recapitulation of encoding fixations during a poststudy, stimulus-free delay period-an effect that has been previously linked to memory maintenance in younger adults-can support mnemonic performance in older adults. Older adults showed greater delay-period fixation reinstatement than younger adults, and this reinstatement supported age-equivalent performance on a subsequent visuospatial-memory-based change detection task, whereas in younger adults, the performance-enhancing effects of fixation reinstatement increased with task difficulty. Taken together, these results suggest that fixation reinstatement might reflect a compensatory response to increased cognitive load. The present findings provide novel evidence of compensatory fixation reinstatement in older adults and demonstrate the utility of eye movement monitoring for aging and memory research. (PsycINFO Database Record

Pupillary responses and memory-guided visual search reveal age-related and Alzheimer's-related memory decline.

Episodic memory - composed of memory for unique spatiotemporal experiences - is known to decline with aging, and even more severely in Alzheimer 's disease (AD). Memory for trial-unique objects in spatial scenes depends on the integrity of the hippocampus and interconnected structures that are among the first areas affected in AD. We reasoned that memory for objects-in-scenes would be impaired with aging, and that further impairments would be observed in AD. We asked younger adults, healthy older adults, older adults at-risk for developing cognitive impairments, and older adults with probable early AD to find changing items ('targets') within images of natural scenes, measuring repeated-trial changes in search efficiency and pupil diameter. Compared to younger adults, older adults took longer to detect target objects in repeated scenes, they required more fixations and those fixations were more dispersed. Whereas individuals with AD showed some benefit of memory in this task, they had substantially longer detection times, and more numerous, dispersed fixations on repeated scenes compared to age-matched older adults. Correspondingly, pupillary responses to novel and repeated scenes were diminished with aging and further in AD, and the memory-related changes were weaker with aging and absent in AD. Our results suggest that several nonverbal measures from memory-guided visual search tasks can index aging and Alzheimer's disease status, including pupillary dynamics. The task measurements are sensitive to the integrity of brain structures that are associated with Alzheimer's-related neurodegeneration, the task is well tolerated across a range of abilities, and thus, it may prove useful in early diagnostics and longitudinal tracking of memory decline.

Selective scanpath repetition during memory-guided visual search.

Visual search efficiency improves with repetition of a search display, yet the mechanisms behind these processing gains remain unclear. According to Scanpath Theory, memory retrieval is mediated by repetition of the pattern of eye movements or "scanpath" elicited during stimulus encoding. Using this framework, we tested the prediction that scanpath recapitulation reflects relational memory guidance during repeated search events. Younger and older subjects were instructed to find changing targets within flickering naturalistic scenes. Search efficiency (search time, number of fixations, fixation duration) and scanpath similarity (repetition) were compared across age groups for novel (V1) and repeated (V2) search events. Younger adults outperformed older adults on all efficiency measures at both V1 and V2, while the search time benefit for repeated viewing (V1-V2) did not differ by age. Fixation-binned scanpath similarity analyses revealed repetition of initial and final (but not middle) V1 fixations at V2, with older adults repeating more initial V1 fixations than young adults. In young adults only, early scanpath similarity correlated negatively with search time at test, indicating increased efficiency, whereas the similarity of V2 fixations to middle V1 fixations predicted poor search performance. We conclude that scanpath compression mediates increased search efficiency by selectively recapitulating encoding fixations that provide goal-relevant input. Extending Scanpath Theory, results suggest that scanpath repetition varies as a function of time and memory integrity.