Deborah E. Hannula

The long and the short of it: relational memory impairments in amnesia, even at short lags.

Classic studies of amnesia led to characterizations of hippocampal function emphasizing involvement in long-term memory rather than short-term (or working) memory. In two experiments, we show that when memory for relations among co-occurring items is tested, hippocampal amnesia results in a deficit even at very short lags. Hence, we find evidence for hippocampal involvement in relational memory, even at short lags normally considered the province of working memory.

Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding

Previous neuropsychological findings have implicated medial temporal lobe (MTL) structures in retaining object-location relations over the course of short delays, but MTL effects have not always been reported in neuroimaging investigations with similar short-term memory requirements. Here, we used event-related functional magnetic resonance imaging to test the hypothesis that the hippocampus and related MTL structures support accurate retention of relational memory representations, even across short delays. On every trial, four objects were presented, each in one of nine possible locations of a three-dimensional grid. Participants were to mentally rotate the grid and then maintain the rotated representation in anticipation of a test stimulus: a rendering of the grid, rotated 90° from the original viewpoint. The test stimulus was either a “match” display, in which object-location relations were intact, or a “mismatch” display, in which one object occupied a new, previously unfilled location (mismatch position), or two objects had swapped locations (mismatch swap). Encoding phase activation in anterior and posterior regions of the left hippocampus, and in bilateral perirhinal cortex, predicted subsequent accuracy on the short-term memory decision, as did bilateral posterior hippocampal activity after the test stimulus. Notably, activation in these posterior hippocampal regions was also sensitive to the degree to which object-location bindings were preserved in the test stimulus; activation was greatest for match displays, followed by mismatch-position displays, and finally mismatch-swap displays. These results indicate that the hippocampus and related MTL structures contribute to successful encoding and retrieval of relational information in visual short-term memory.

The Eyes Have It: Hippocampal Activity Predicts Expression of Memory in Eye Movements

Although there is widespread agreement that the hippocampus is critical for explicit episodic memory retrieval, it is controversial whether this region can also support indirect expressions of relational memory when explicit retrieval fails. Here, using functional magnetic resonance imaging (fMRI) with concurrent indirect, eye-movement-based memory measures, we obtained evidence that hippocampal activity predicted expressions of relational memory in subsequent patterns of viewing, even when explicit, conscious retrieval failed. Additionally, activity in the lateral prefrontal cortex and functional connectivity between the hippocampus and prefrontal cortex were greater for correct than for incorrect trials. Together, these results suggest that hippocampal activity can support the expression of relational memory even when explicit retrieval fails and that recruitment of a broader cortical network may be required to support explicit associative recognition.

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.

Imaging implicit perception: promise and pitfalls

The study of implicit perception — perception in the absence of awareness — has a long history. Decades of behavioural work have identified crucial theoretical and methodological issues that must be considered when evaluating claims of implicit perception. Neuroimaging methods provide an important new avenue for illuminating our understanding of perception both with and without awareness, but most imaging experiments have not met the rigorous conditions that the behavioural work has shown are necessary for inferring implicit perception. Here, we review the literature of both behavioural and neuroimaging studies, and note the pitfalls of studying implicit perception as well as the promise that neuroimaging studies have for providing insights about implicit perception when combined with appropriately rigorous behavioural measures of awareness.

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.

The hippocampus reevaluated in unconscious learning and memory: at a tipping point?

Classic findings from the neuropsychological literature invariably indicated that performances on tests of memory that can be accomplished without conscious awareness were largely spared in amnesia, while those that required conscious retrieval (e.g., via recognition or recall) of information learned in the very same sessions was devastatingly impaired. Based on reports of such dissociations, it was proposed that one of the fundamental distinctions between memory systems is whether or not they support conscious access to remembered content. Only recently have we come to realize that the putative systemic division of labor between conscious and unconscious memory is not so clean. A primary goal of this review is to examine recent evidence that has been advanced against the view that the hippocampus is selectively critical for conscious memory. Along the way, consideration is given to criticisms that have been levied against these findings, potential explanations for differences in the reported results are proposed, and methodological pitfalls in investigations of unconscious memory are discussed. Ultimately, it is concluded that a tipping point has been reached, and that while conscious recollection depends critically on hippocampal integrity, the reach of the hippocampus extends to unconscious aspects of memory performance when relational memory processing and representation are required.

The Eyes Know Eye Movements as a Veridical Index of Memory

In two experiments, we examined whether observers’ eye movements distinguish studied faces from highly similar novel faces. Participants’ eye movements were monitored while they viewed three-face displays. Target-present displays contained a studied face and two morphed faces that were visually similar to it; target-absent displays contained three morphed faces that were visually similar to a studied, but not tested, face. On each trial in a test session, participants were instructed to choose the studied face if it was present or a random face if it was not and then to indicate whether the chosen face was studied. Whereas manipulating visual similarity in target-absent displays influenced the rate of false endorsements of nonstudied items as studied, eye movements proved impervious to this manipulation. Studied faces were viewed disproportionately from 1,000 to 2,000 ms after display onset and from 1,000 to 500 ms before explicit identification. Early viewing also distinguished studied faces from faces incorrectly endorsed as studied. Our findings show that eye movements provide a relatively pure index of past experience that is uninfluenced by explicit response strategies, and suggest that eye movement measures may be of practical use in applied settings.

Medial temporal lobe coding of item and spatial information during relational binding in working memory

Several models have proposed that different medial temporal lobe (MTL) regions represent different kinds of information in the service of long-term memory. For instance, it has been proposed that perirhinal cortex (PRC), parahippocampal cortex (PHC), and hippocampus differentially support long-term memory for item information, spatial context, and item–context relations present during an event, respectively. Recent evidence has indicated that, in addition to long-term memory, MTL subregions may similarly contribute to processes that support the retention of complex spatial arrangements of objects across short delays. Here, we used functional magnetic resonance imaging and multivoxel pattern similarity analysis to investigate the extent to which human MTL regions independently code for object and spatial information, as well as the conjunction of this information, during working memory encoding and active maintenance. Voxel activity patterns in PRC, temporopolar cortex, and amygdala carried information about individual objects, whereas activity patterns in the PHC and posterior hippocampus carried information about the configuration of spatial locations that was to be remembered. Additionally, the integrity of multivoxel patterns in the right anterior hippocampus across encoding and delay periods was predictive of accurate short-term memory for object–location relationships. These results are consistent with parallel processing of item and spatial context information by PRC and PHC, respectively, and the binding of item and context by the hippocampus.

Medial temporal lobe contributions to cued retrieval of items and contexts.

Several models have proposed that different regions of the medial temporal lobes contribute to different aspects of episodic memory. For instance, according to one view, the perirhinal cortex represents specific items, parahippocampal cortex represents information regarding the context in which these items were encountered, and the hippocampus represents item-context bindings. Here, we used event-related functional magnetic resonance imaging (fMRI) to test a specific prediction of this model-namely, that successful retrieval of items from context cues will elicit perirhinal recruitment and that successful retrieval of contexts from item cues will elicit parahippocampal cortex recruitment. Retrieval of the bound representation in either case was expected to elicit hippocampal engagement. To test these predictions, we had participants study several item-context pairs (i.e., pictures of objects and scenes, respectively), and then had them attempt to recall items from associated context cues and contexts from associated item cues during a scanned retrieval session. Results based on both univariate and multivariate analyses confirmed a role for hippocampus in content-general relational memory retrieval, and a role for parahippocampal cortex in successful retrieval of contexts from item cues. However, we also found that activity differences in perirhinal cortex were correlated with successful cued recall for both items and contexts. These findings provide partial support for the above predictions and are discussed with respect to several models of medial temporal lobe function.