Concerns about confounds: False memory as an explanation for a hippocampus-supported implicit eye-movement-based relational memory effect.

Steinkrauss and Slotnick (2024) propose that implicit eye-movement-based relational memory effects, predicted by hippocampal activity differences (Hannula & Ranganath, 2009), are due to an explicit false memory confound. However, the logic behind this claim is insufficiently fleshed out and alternative accounts of how false memory may have played out in this task were not considered. One such account would predict a pattern of results counter to the observed fMRI results, and another would be consistent with our original conclusions. These alternatives are described along with converging evidence from an additional fMRI study that was not considered by Steinkrauss and Slotnick.

Control of memory retrieval alters memory-based eye movements.

Past work has shown that eye movements are affected by long-term memory across different tasks and instructional manipulations. In the current study, we tested whether these memory-based eye movements persist when memory retrieval is under intentional control. Participants encoded multiple scenes with six objects (three faces; three tools). Next, they completed a memory regulation and visual search task, while undergoing eye tracking. Here, scene cues were presented and participants either retrieved the encoded associate, suppressed it, or substituted it with a specific object from the other encoded category. Following a delay, a search display consisting of six dots intermixed with the six encoded objects was presented. Participants' task was to fixate one remaining dot after five had disappeared. Incidental viewing of the objects was of interest. Results revealed that performance in a final recognition phase was impaired for suppressed pairs, but only when the associate was a tool. During the search task, incidental associate viewing was lower when participants attempted to control retrieval, whereas one object from the nonassociate category was most viewed in the substitute condition. Additionally, viewing patterns in the search phase were related to final recognition performance, but the direction of this association differed between conditions. Overall, these results suggest that eye movements are attracted to information retrieved from long-term memory and held active (the associate in the retrieve condition, or an object from the other category in the substitute condition). Furthermore, the level of viewing may index the strength of the representation of retrieved information. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Relational memory weakness in autism despite the use of a controlled encoding task.

Introduction: Recent work challenged past findings that documented relational memory impairments in autism. Previous studies often relied solely on explicit behavioral responses to assess relational memory integrity, but successful performance on behavioral tasks may rely on other cognitive abilities (e.g., executive functioning) that are impacted in some autistic individuals. Eye-tracking tasks do not require explicit behavioral responses, and, further, eye movements provide an indirect measure of memory. The current study examined whether memory-specific viewing patterns toward scenes differ between autistic and non-autistic individuals. Methods: Using a long-term memory paradigm that equated for complexity between item and relational memory tasks, participants studied a series of scenes. Following the initial study phase, scenes were re-presented, accompanied by an orienting question that directed participants to attend to either features of an item (i.e., in the item condition) or spatial relationships between items (i.e., in the relational condition) that might be subsequently modified during test. At test, participants viewed scenes that were unchanged (i.e., repeated from study), scenes that underwent an "item" modification (an exemplar switch) or a "relational" modification (a location switch), and scenes that had not been presented before. Eye movements were recorded throughout. Results: During study, there were no significant group differences in viewing directed to regions of scenes that might be manipulated at test, suggesting comparable processing of scene details during encoding. However, there was a group difference in explicit recognition accuracy for scenes that underwent a relational change. Marginal group differences in the expression of memory-based viewing effects during test for relational scenes were consistent with this behavioral outcome, particularly when analyses were limited to scenes recognized correctly with high confidence. Group differences were also evident in correlational analyses that examined the association between study phase viewing and recognition accuracy and between performance on the Picture Sequence Memory Test and recognition accuracy. Discussion: Together, our findings suggest differences in the integrity of relational memory representations and/or in the relationships between subcomponents of memory in autism.

Conscious awareness and memory systems in the brain.

The term "memory" typically refers to conscious retrieval of events and experiences from our past, but experience can also change our behaviour without corresponding awareness of the learning process or the associated outcome. Based primarily on early neuropsychological work, theoretical perspectives have distinguished between conscious memory, said to depend critically on structures in the medial temporal lobe (MTL), and a collection of performance-based memories that do not. The most influential of these memory systems perspectives, the declarative memory theory, continues to be a mainstay of scientific work today despite mounting evidence suggesting that contributions of MTL structures go beyond the kinds or types of memory that can be explicitly reported. Consistent with these reports, more recent perspectives have focused increasingly on the processing operations supported by particular brain regions and the qualities or characteristics of resulting representations whether memory is expressed with or without awareness. These alternatives to the standard model generally converge on two key points. First, the hippocampus is critical for relational memory binding and representation even without awareness and, second, there may be little difference between some types of priming and explicit, familiarity-based recognition. Here, we examine the evolution of memory systems perspectives and critically evaluate scientific evidence that has challenged the status quo. Along the way, we highlight some of the challenges that researchers encounter in the context of this work, which can be contentious, and describe innovative methods that have been used to examine unconscious memory in the lab. This article is categorized under: Psychology > Memory Psychology > Theory and Methods Philosophy > Consciousness.

Contextual cueing is not flexible.

Target detection is faster when search displays repeat, but properties of the memory representations that give rise to this contextual cueing effect remain uncertain. We adapted the contextual cueing task using an ABA design and recorded the eye movements of healthy young adults to determine whether the memory representations are flexible. Targets moved to a new location during the B phase and then returned to their original locations (second A phase). Contextual cueing effects in the first A phase were reinstated immediately in the second A phase, and response time costs eventually gave way to a repeated search advantage in the B phase, suggesting that two target-context associations were learned. However, this apparent flexibility disappeared when eye tracking data were used to subdivide repeated displays based on B-phase viewing of the original target quadrant. Therefore, memory representations acquired in the contextual cueing task resist change and are not flexible.

Temporal Regularity May Not Improve Memory for Item-Specific Detail.

Regularities in event timing allow for the allocation of attention to critical time-points when an event is most likely to occur, leading to improved visual perception. Results from recent studies indicate that similar benefits may extend to memory for scenes and objects. Here, we investigated whether benefits of temporal regularity are evident when detailed, item-specific representations are necessary for successful recognition memory performance. In Experiments 1 and 2, pictures of objects were presented with either predictable or randomized event timing, in separate encoding blocks. In the test phase, old and new objects were presented, intermixed with perceptually similar exemplars of encoded objects. In Experiment 3 we attempted to replicate previously reported memory enhancements for scenes. In contrast to predictions, temporal regularity did not affect response times (RT) or improve recognition memory accuracy in any of our experiments. These results suggest that any effects of temporal expectation on memory are subtle and may be sensitive to minor changes in task parameters. In sum, indirect upregulation of attention through imposed temporal structure may not be sufficient to have downstream effects on memory performance.

Attention capture by episodic long-term memory.

Everyday behavior depends upon the operation of concurrent cognitive processes. In visual search, studies that examine memory-attention interactions have indicated that long-term memory facilitates search for a target (e.g., contextual cueing), but the potential for memories to capture attention and decrease search efficiency has not been investigated. To address this gap in the literature, five experiments were conducted to examine whether task-irrelevant encoded objects might capture attention. In each experiment, participants encoded scene-object pairs. Then, in a visual search task, 6-object search displays were presented and participants were told to make a single saccade to targets defined by shape (e.g., diamond among differently colored circles; Experiments 1, 4, and 5) or by color (e.g., blue shape among differently shaped gray objects; Experiments 2 and 3). Sometimes, one of the distractors was from the encoded set, and occasionally the scene that had been paired with that object was presented prior to the search display. Results indicated that eye movements were made, in error, more often to encoded distractors than to baseline distractors, and that this effect was greatest when the corresponding scene was presented prior to search. When capture did occur, participants looked longer at encoded distractors if scenes had been presented, an effect that we attribute to the representational match between a retrieved associate and the identity of the encoded distractor in the search display. In addition, the presence of a scene resulted in slower saccade deployment when participants made first saccades to targets, as instructed. Experiments 4 and 5 suggest that this slowdown may be due to the relatively rare and therefore, surprising, appearance of visual stimulus information prior to search. Collectively, results suggest that information encoded into episodic memory can capture attention, which is consistent with the recent proposal that selection history can guide attentional selection.

Subliminal encoding and flexible retrieval of objects in scenes.

Our episodic memory stores what happened when and where in life. Episodic memory requires the rapid formation and flexible retrieval of where things are located in space. Consciousness of the encoding scene is considered crucial for episodic memory formation. Here, we question the necessity of consciousness and hypothesize that humans can form unconscious episodic memories. Participants were presented with subliminal scenes, that is, scenes invisible to the conscious mind. The scenes displayed objects at certain locations for participants to form unconscious object-in-space memories. Later, the same scenes were presented supraliminally, that is, visibly, for retrieval testing. Scenes were presented absent the objects and rotated by 90°-270° in perspective to assess the representational flexibility of unconsciously formed memories. During the test phase, participants performed a forced-choice task that required them to place an object in one of two highlighted scene locations and their eye movements were recorded. Evaluation of the eye tracking data revealed that participants remembered object locations unconsciously, irrespective of changes in viewing perspective. This effect of gaze was related to correct placements of objects in scenes, and an intuitive decision style was necessary for unconscious memories to influence intentional behavior to a significant degree. We conclude that conscious perception is not mandatory for spatial episodic memory formation.

Eye movements are captured by a perceptually simple conditioned stimulus in the absence of explicit contingency knowledge.

Past reports suggest that threatening materials can impact the efficiency of goal-directed behavior. However, questions remain about whether a conditional stimulus (CS) can capture attention as previous results may have been influenced by voluntary prioritization of a to-be-ignored CS. In 2 experiments, eye tracking was used to evaluate whether neutral, perceptually simple materials capture attention when they take on aversive properties via probabilistic fear conditioning with strict methods in place to eliminate voluntary CS prioritization. During training, participants attempted to fixate search targets (i.e., horizontally or vertically oriented rectangles) as quickly as possible to avoid shock. In reality, shock administration was related to rectangle orientation so that 1 rectangle (CS+) predicted shock more often than the other (CS-). Subsequently rectangles became distractors and were to be ignored. At this point, participants were instructed to fixate a new target and incidences of CS capture were examined. Results showed that saccades were made more quickly to the CS+ than the CS- as training progressed, and that oculomotor capture by irrelevant rectangles occurred more often for the CS+ than the CS-. An independent physiological index (skin conductance response) confirmed that contingencies had been learned, as SCR magnitude was greater for CS+ than CS- trials early in the test phase. These effects were documented despite the absence of explicit contingency knowledge, assessed using a postexperimental questionnaire. Collectively, these outcomes indicate that a CS can capture attention despite being task-irrelevant, and that these effects do not depend on conscious awareness of learned contingencies. (PsycINFO Database Record

Eye Movements Index Implicit Memory Expression in Fear Conditioning.

The role of contingency awareness in simple associative learning experiments with human participants is currently debated. Since prior work suggests that eye movements can index mnemonic processes that occur without awareness, we used eye tracking to better understand the role of awareness in learning aversive Pavlovian conditioning. A complex real-world scene containing four embedded household items was presented to participants while skin conductance, eye movements, and pupil size were recorded. One item embedded in the scene served as the conditional stimulus (CS). One exemplar of that item (e.g. a white pot) was paired with shock 100 percent of the time (CS+) while a second exemplar (e.g. a gray pot) was never paired with shock (CS-). The remaining items were paired with shock on half of the trials. Participants rated their expectation of receiving a shock during each trial, and these expectancy ratings were used to identify when (i.e. on what trial) each participant became aware of the programmed contingencies. Disproportionate viewing of the CS was found both before and after explicit contingency awareness, and patterns of viewing distinguished the CS+ from the CS-. These observations are consistent with "dual process" models of fear conditioning, as they indicate that learning can be expressed in patterns of viewing prior to explicit contingency awareness.

Relational Memory Is Evident in Eye Movement Behavior despite the Use of Subliminal Testing Methods.

While it is generally agreed that perception can occur without awareness, there continues to be debate about the type of representational content that is accessible when awareness is minimized or eliminated. Most investigations that have addressed this issue evaluate access to well-learned representations. Far fewer studies have evaluated whether or not associations encountered just once prior to testing might also be accessed and influence behavior. Here, eye movements were used to examine whether or not memory for studied relationships is evident following the presentation of subliminal cues. Participants assigned to experimental or control groups studied scene-face pairs and test trials evaluated implicit and explicit memory for these pairs. Each test trial began with a subliminal scene cue, followed by three visible studied faces. For experimental group participants, one face was the studied associate of the scene (implicit test); for controls none were a match. Subsequently, the display containing a match was presented to both groups, but now it was preceded by a visible scene cue (explicit test). Eye movements were recorded and recognition memory responses were made. Participants in the experimental group looked disproportionately at matching faces on implicit test trials and participants from both groups looked disproportionately at matching faces on explicit test trials, even when that face had not been successfully identified as the associate. Critically, implicit memory-based viewing effects seemed not to depend on residual awareness of subliminal scene cues, as subjective and objective measures indicated that scenes were successfully masked from view. The reported outcomes indicate that memory for studied relationships can be expressed in eye movement behavior without awareness.

Impaired recollection of visual scene details in adults with autism spectrum conditions.

Subtle memory deficits observed in autism spectrum conditions (ASC) have often been characterized as reflecting impaired recollection and it has been proposed that a relational binding deficit may underlie the recollection impairment. However, subjective recollection and relational binding have not been measured within the same task in ASC to date and it is unclear whether a relational binding deficit can provide a full account of recollection impairments in ASC. Relational memory has also not been compared with item memory when the demands of the 2 tasks are comparable. To assess recollection, relational memory, and item memory within a single task in ASC, 24 adults with ASC and 24 typically developed adults undertook a change detection memory task that assessed recollection of item-specific and spatial details. Participants studied rendered indoor and outdoor scenes and, in a subsequent recognition memory test, distinguished scenes that had not changed from those that had either undergone an item change (a different item exemplar) or a relational (spatial) change, which was followed by a subjective recollection judgment. The ASC group identified fewer item changes and spatial changes, to a similar degree, which was attributable to a specific reduction in recollection-based recognition relative to the control group. These findings provide evidence that recollection deficits in ASC may not be driven entirely by a relational binding deficit.

Memory for items and relationships among items embedded in realistic scenes: disproportionate relational memory impairments in amnesia.

OBJECTIVE: The objective of this study was to examine the dependence of item memory and relational memory on medial temporal lobe (MTL) structures. Patients with amnesia, who either had extensive MTL damage or damage that was relatively restricted to the hippocampus, were tested, as was a matched comparison group. Disproportionate relational memory impairments were predicted for both patient groups, and those with extensive MTL damage were also expected to have impaired item memory. METHOD: Participants studied scenes, and were tested with interleaved 2-alternative forced-choice probe trials. Probe trials were either presented immediately after the corresponding study trial (Lag 1), 5 trials later (Lag 5), or 9 trials later (Lag 9) and consisted of the studied scene along with a manipulated version of that scene in which 1 item was replaced with a different exemplar (item memory test) or was moved to a new location (relational memory test). Participants were to identify the exact match of the studied scene. RESULTS: As predicted, patients were disproportionately impaired on the test of relational memory. Item memory performance was marginally poorer among patients with extensive MTL damage, but both groups were impaired relative to matched comparison participants. Impaired performance was evident at all lags, including the shortest possible lag (Lag 1). CONCLUSIONS: The results are consistent with the proposed role of the hippocampus in relational memory binding and representation, even at short delays, and suggest that the hippocampus may also contribute to successful item memory when items are embedded in complex scenes.

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.

Short-term retention of relational memory in amnesia revisited: accurate performance depends on hippocampal integrity.

Traditionally, it has been proposed that the hippocampus and adjacent medial temporal lobe cortical structures are selectively critical for long-term declarative memory, which entails memory for inter-item and item-context relationships. Whether the hippocampus might also contribute to short-term retention of relational memory representations has remained controversial. In two experiments, we revisit this question by testing memory for relationships among items embedded in scenes using a standard working memory trial structure in which a sample stimulus is followed by a brief delay and the corresponding test stimulus. In each experimental block, eight trials using different exemplars of the same scene were presented. The exemplars contained the same items but with different spatial relationships among them. By repeating the pictures across trials, any potential contributions of item or scene memory to performance were minimized, and relational memory could be assessed more directly than has been done previously. When test displays were presented, participants indicated whether any of the item-location relationships had changed. Then, regardless of their responses (and whether any item did change its location), participants indicated on a forced-choice test, which item might have moved, guessing if necessary. Amnesic patients were impaired on the change detection test, and were frequently unable to specify the change after having reported correctly that a change had taken place. Comparison participants, by contrast, frequently identified the change even when they failed to report the mismatch, an outcome that speaks to the sensitivity of the change specification measure. These results confirm past reports of hippocampal contributions to short-term retention of relational memory representations, and suggest that the role of the hippocampus in memory has more to do with relational memory requirements than the length of a retention interval.

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.

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.

Distinguishing highly confident accurate and inaccurate memory: insights about relevant and irrelevant influences on memory confidence.

It is generally believed that accuracy and confidence in one's memory are related, but there are many instances when they diverge. Accordingly it is important to disentangle the factors that contribute to memory accuracy and confidence, especially those factors that contribute to confidence, but not accuracy. We used eye movements to separately measure fluent cue processing, the target recognition experience, and relative evidence assessment on recognition confidence and accuracy. Eye movements were monitored during a face-scene associative recognition task, in which participants first saw a scene cue, followed by a forced-choice recognition test for the associated face, with confidence ratings. Eye movement indices of the target recognition experience were largely indicative of accuracy, and showed a relationship to confidence for accurate decisions. In contrast, eye movements during the scene cue raised the possibility that more fluent cue processing was related to higher confidence for both accurate and inaccurate recognition decisions. In a second experiment we manipulated cue familiarity, and therefore cue fluency. Participants showed higher confidence for cue-target associations for when the cue was more familiar, especially for incorrect responses. These results suggest that over-reliance on cue familiarity and under-reliance on the target recognition experience may lead to erroneous confidence.