Jennifer D. Ryan

Amnesia is a Deficit in Relational Memory

Eye movements were monitored to assess memory for scenes indirectly (implicitly). Two eye movement—based memory phenomena were observed: (a) the repetition effect, a decrease in sampling of previously viewed scenes compared with new scenes, reflecting memory for those scenes, and (b) the relational manipulation effect, an increase in viewing of the regions where manipulations of relations among scene elements had occurred. In normal control subjects, the relational manipulation effect was expressed only in the absence of explicit awareness of the scene manipulations. Thus, memory representations of scenes contain information about relations among elements of the scenes, at least some of which is not accessible to verbal report. But amnesic patients with severe memory impairment failed to show the relational manipulation effect. Their failure to show any demonstrable memory for relations among the constituent elements of scenes suggests that amnesia involves a fundamental deficit in relational (declarative) memory processing.

Angry, Disgusted, or Afraid? Studies on the Malleability of Emotion Perception

Current theories of emotion perception posit that basic facial expressions signal categorically discrete emotions or affective dimensions of valence and arousal. In both cases, the information is thought to be directly “read out” from the face in a way that is largely immune to context. In contrast, the three studies reported here demonstrated that identical facial configurations convey strikingly different emotions and dimensional values depending on the affective context in which they are embedded. This effect is modulated by the similarity between the target facial expression and the facial expression typically associated with the context. Moreover, by monitoring eye movements, we demonstrated that characteristic fixation patterns previously thought to be determined solely by the facial expression are systematically modulated by emotional context already at very early stages of visual processing, even by the first time the face is fixated. Our results indicate that the perception of basic facial expressions is not context invariant and can be categorically altered by context at early perceptual levels.

Worth a Glance: Using Eye Movements to Investigate the Cognitive Neuroscience of Memory

Results of several investigations indicate that eye movements can reveal memory for elements of previous experience. These effects of memory on eye movement behavior can emerge very rapidly, changing the efficiency and even the nature of visual processing without appealing to verbal reports and without requiring conscious recollection. This aspect of eye movement based memory investigations is particularly useful when eye movement methods are used with special populations (e.g., young children, elderly individuals, and patients with severe amnesia), and also permits use of comparable paradigms in animals and humans, helping to bridge different memory literatures and permitting cross-species generalizations. Unique characteristics of eye movement methods have produced findings that challenge long-held views about the nature of memory, its organization in the brain, and its failures in special populations. Recently, eye movement methods have been successfully combined with neuroimaging techniques such as fMRI, single-unit recording, and magnetoencephalography, permitting more sophisticated investigations of memory. Ultimately, combined use of eye-tracking with neuropsychological and neuroimaging methods promises to provide a more comprehensive account of brain–behavior relationships and adheres to the “converging evidence” approach to cognitive neuroscience.

The hippocampus supports multiple cognitive processes through relational binding and comparison.

It has been well established that the hippocampus plays a pivotal role in explicit long-term recognition memory. However, findings from amnesia, lesion and recording studies with non-human animals, eye-movement recording studies, and functional neuroimaging have recently converged upon a similar message: the functional reach of the hippocampus extends far beyond explicit recognition memory. Damage to the hippocampus affects performance on a number of cognitive tasks including recognition memory after short and long delays and visual discrimination. Additionally, with the advent of neuroimaging techniques that have fine spatial and temporal resolution, findings have emerged that show the elicitation of hippocampal responses within the first few 100 ms of stimulus/task onset. These responses occur for novel and previously viewed information during a time when perceptual processing is traditionally thought to occur, and long before overt recognition responses are made. We propose that the hippocampus is obligatorily involved in the binding of disparate elements across both space and time, and in the comparison of such relational memory representations. Furthermore, the hippocampus supports relational binding and comparison with or without conscious awareness for the relational representations that are formed, retrieved and/or compared. It is by virtue of these basic binding and comparison functions that the reach of the hippocampus extends beyond long-term recognition memory and underlies task performance in multiple cognitive domains.

Processing and short-term retention of relational information in amnesia.

In a recent eye-movement study [Psychol. Sci. 11 (2000) 454], amnesic patients failed selectively to exhibit long-term effects of memory for the relations among the constituent elements of scenes. This failure could be due to a deficit specifically in long-term relational memory, as we have suggested; or in retention of relational information over any delay, whether involving perceptual processing and short-term maintenance or long-term memory, consistent with suggestions from recent studies of the hippocampus; or in on-line processing of relational information, as would occur in perceptual or feature binding. Here we show robust eye-movement effects of relations among elements of scenes in amnesia in a short-delay matching task, with the same materials and in the same amnesic patients in which long-delay conditions elicited failure. These findings document intact processing and short-term retention of relational information in amnesia, indicating that amnesia associated with hippocampal damage results in a relational memory deficit, specifically of long-term memory.

The obligatory effects of memory on eye movements

Previous work has shown that eye movement behaviour is affected by previous experience, such that alterations in viewing patterns can be observed to previously viewed compared to novel displays. The current work addresses the extent to which such effects of memory on eye movement behaviour are obligatory; that is, we examined whether prior experience could alter subsequent eye movement behaviour under a variety of testing conditions, for stimuli that varied on the nature of the prior exposure. While task demands influenced whether viewing was predominantly directed to the novel versus familiar faces, viewing of the familiar faces was distinguished from viewing of the novel faces, regardless of whether the task required incidental encoding or intentional retrieval. Changes in scanning of previously viewed over novel faces emerged early in viewing; in particular, viewing duration of the first fixation to the familiar faces was often significantly different from the duration of the first fixation directed to the novel faces, regardless of whether prior exposure was solely in the context of the experiment or due to real-world exposure. These findings suggest that representations maintained in memory may be retrieved and compared with presented information obligatorily.

Eyes always attract attention but gaze orienting is task-dependent: evidence from eye movement monitoring.

Eyes and gaze are central to social cognition but whether they attract attention differently depending on the task is unknown. Here, the shift in attention towards the eye region and gaze direction of a perceived face was studied in two tasks by monitoring eye movements. The same face stimuli in front- or 3/4-view, with direct or averted gaze, were used in both tasks. In the Gaze task, subjects performed an explicit gaze direction judgment (gaze straight or averted) while in the Head task they performed a head orientation judgment (front- or 3/4-view). Gaze processing was evident in both tasks as shown by longer RTs and lower accuracy when head and gaze directions did not match. In both tasks the eye region was the most attended area but the amount of viewing was task-dependent. Most importantly, approximately 90% of the initial saccades landed in the eye region in the Gaze task but only approximately 50% of them did so in the Head task. These saccades were made in the direction signaled by gaze in the Gaze task but in the direction signaled by head orientation in the Head task. Altogether, these task-modulated behaviors argue against a purely exogenous and automatic orienting-to-gaze mechanism. Based on patient work and neuroimaging studies of gaze processing, we suggest that this task-dependent orienting behavior is rather endogenous and subtended by cortical areas amongst which frontal regions play a central role. We discuss the implications of this finding for clinical populations.

Age-Related Deficits in Face Recognition are Related to Underlying Changes in Scanning Behavior

ABSTRACT Previous studies demonstrating age-related impairments in recognition memory for faces are suggestive of underlying differences in face processing. To study these differences, we monitored eye movements while younger and older adults viewed younger and older faces. Compared to the younger group, older adults showed increased sampling of facial features, and more transitions. However, their scanning behavior was most similar to the younger group when looking at older faces. Moreover, while older adults exhibited worse recognition memory than younger adults overall, their memory was more accurate for older faces. These findings suggest that age-related differences in recognition memory for faces may be related to changes in scanning behavior, and that older adults may use social group status as a compensatory processing strategy.

A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography

Neuropsychological and neuroimaging findings reveal that the hippocampus is important for recognition memory. However, it is unclear when and whether the hippocampus contributes differentially to recognition of previously studied items (old) versus novel items (new), or contributes to a general processing requirement that is necessary for recognition of both types of information. To address this issue, we examined the temporal dynamics and spectral frequency underlying hippocampal activity during recognition of old/new complex scenes using magnetoencephalography (MEG). In order to provide converging evidence to existing literature in support of the potential of MEG to localize the hippocampus, we reconstructed brain source activity using the beamformer method and analyzed three types of processing-related signal changes by applying three different analysis methods: (1) Synthetic aperture magnetometry (SAM) revealed event related and non-event-related spectral power changes; (2) Inter-trial coherence (ITC) revealed time-locked changes in neural synchrony; and (3) Event-related SAM (ER-SAM) revealed averaged event-related responses over time. Hippocampal activity was evident for both old and new information within the theta frequency band and during the first 250 ms following stimulus onset. The early onset of hippocampal responses suggests that general comparison processes related to recognition of new/old information may occur obligatorily.

Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships.

This study examined contributions of the hippocampus, amygdala and perirhinal cortex to memory. Rats performed a cover task, and changes to stimulus identity or relationships were used to test incidental memory. Rats with hippocampal damage showed deficient responses to relationship changes, but demonstrated knowledge of the position and identity of the target object. They over-focused on the most predictive stimuli, and failed to acquire associations including surrounding cues. Rats with amygdala damage responded to changes involving distal stimuli, and showed deficient responses to novel objects and object relationships. These rats may be highly reliant on relational representations, resulting in a reduced salience for individual novel stimuli. Rats with perirhinal damaged responded to novel stimulus relationships and distal cues, but showed deficient responses to novel objects, suggesting that changes in identity had reduced salience. Implications for declarative and conjunctive hippocampal theories are discussed.