Caitlin R. Bowman

True and phantom recollection: an fMRI investigation of similar and distinct neural correlates and connectivity.

Although research suggests that most false memories are mediated by a sense of familiarity, behavioral evidence indicates that some are characterized by retrieval of item-specific details associated with recollection. However, neuroimaging studies have yet to isolate and analyze the neural correlates of false (or phantom) recollection, focusing instead on general recognition processes. In doing so, results are mixed with respect to the role of the medial temporal lobes (MTL) in distinguishing between true and false retrieval. The present study sought to investigate the neural basis of true and phantom recollection and clarify the role of the MTL in dissociating between the two processes. Results showed that true and phantom recollection were associated with a largely overlapping retrieval network including activity in bilateral anterior parahippocampal gyrus, fusiform gyrus, anterior cingulate cortex, and right superior parietal cortex. However, connectivity analyses using two common MTL seeds revealed a more inferior network (fusiform gyrus, hippocampus, middle temporal gyrus) associated with true recollection and a more superior network (superior parietal, superior frontal gyrus, posterior cingulate cortex) associated with false recollection. Finally, direct comparisons between true and phantom recollection showed greater activity in right hippocampus and early visual cortex for true recollection, whereas no region exhibited greater activity for false recollection. Results indicate that while both true and phantom recollection show similar patterns of activation, there are also distinctions in the neural networks contributing to the two recollection processes. Moreover, results conclude that within the MTL, the hippocampus proper can distinguish between true and phantom recollection.

Age-related differences in the neural correlates mediating false recollection

The current study investigated the effects of aging on the neural basis underlying true and false recollection. Although older adults, compared with younger adults, exhibited equivalent rates of true recollection, age differences in true recollection showed a pattern of activity commonly found among previous memory studies (e.g., age-related decreases in occipital and increases in prefrontal cortices), suggesting reduced retrieval of perceptual details associated with encoding items and a greater reliance on top-down compensatory processing. With regard to false recollection, older adults exhibited significantly greater false recollection yet did not exhibit increased neural processing. They did exhibit decreased activity in prefrontal, parahippocampal gyrus, and occipitoparietal cortex, suggesting a reduced reliance on reconstruction processes mediating false recollection in young. An individual differences analysis in older adults found false recollection rates predicted activity in several regions. including bilateral middle/superior temporal gyrus. Taken together, these results indicate that increases in false recollection in aging may be mediated by reduced access to encoding-related details as well as reliance on semantic gist and familiarity-related neural activity.

Age differences in the neural correlates of novelty processing: The effects of item-relatedness

Past research finds that age-related increases in false recognitions are a key contributor to age-related memory decline, suggesting that older adults have difficulty in correctly distinguishing between new and old information, particularly when new items at retrieval are semantically or perceptually related to items from encoding. However, little work has examined the neural mechanisms older adults engage to avoid false recognitions and successfully identify information as novel. In the present study, young and older adults were scanned during a retrieval task in which new items were exemplars from studied categories (related lures) or unstudied categories (unrelated lures) in order to detect age-related differences in the neural correlates of related and unrelated novelty processing. Results showed that, unlike young adults, older adults did not differentially recruit regions such as the anterior cingulate and bilateral middle/inferior temporal gyrus to capitalize on the salient categorical differences in unrelated items. Likewise, older adults did not differentially recruit regions of early visual cortex or anterior hippocampus, suggesting that older adults have difficulty using item-specific details to make successful related novelty decisions. Instead, older adults recruited bilateral ventrolateral prefrontal cortex differentially for successful novelty processing and particularly for related novelty processing. Overall, results suggest that age deficits in novelty processing may arise because older adults process related and unrelated lures similarly and do not capitalize on categorical or item-specific properties of novel items. Similar to aging patterns in memory retrieval, results also showed that older adults have the strongest novelty success activity in lateral PFC regions associated with control and monitoring processes. This article is part of a Special Issue entitled SI: Memory & Aging.

The neural basis of recollection rejection: Increases in hippocampal-prefrontal connectivity in the absence of a shared recall-to-reject and target recollection network

Recollection rejection or “recall-to-reject” is a mechanism that has been posited to help maintain accurate memory by preventing the occurrence of false memories. Recollection rejection occurs when the presentation of a new item during recognition triggers recall of an associated target, a mismatch in features between the new and old items is registered, and the lure is correctly rejected. Critically, this characterization of recollection rejection involves a recall signal that is conceptually similar to recollection as elicited by a target. However, previous neuroimaging studies have not evaluated the extent to which recollection rejection and target recollection rely on a common neural signal but have instead focused on recollection rejection as a postretrieval monitoring process. This study utilized a false memory paradigm in conjunction with an adapted remember–know–new response paradigm that separated “new” responses based on recollection rejection from those that were based on a lack of familiarity with the item. This procedure allowed for parallel recollection rejection and target recollection contrasts to be computed. Results revealed that, contrary to predictions from theoretical and behavioral literature, there was virtually no evidence of a common retrieval mechanism supporting recollection rejection and target recollection. Instead of the typical target recollection network, recollection rejection recruited a network of lateral prefrontal and bilateral parietal regions that is consistent with the retrieval monitoring network identified in previous neuroimaging studies of recollection rejection. However, a functional connectivity analysis revealed a component of the frontoparietal rejection network that showed increased coupling with the right hippocampus during recollection rejection responses. As such, we demonstrate a possible link between PFC monitoring network and basic retrieval mechanisms within the hippocampus that was not revealed with univariate analyses alone.

The neural correlates of correctly rejecting lures during memory retrieval: the role of item relatedness

Successful memory retrieval is predicated not only on recognizing old information, but also on correctly rejecting new information (lures) in order to avoid false memories. Correctly rejecting lures is more difficult when they are perceptually or semantically related to information presented at study as compared to when lures are distinct from previously studied information. This behavioral difference suggests that the cognitive and neural basis of correct rejections differs with respect to the relatedness between lures and studied items. The present study sought to identify neural activity that aids in suppressing false memories by examining the network of brain regions underlying correct rejection of related and unrelated lures. Results showed neural overlap in the right hippocampus and anterior parahippocampal gyrus associated with both related and unrelated correct rejections, indicating that some neural regions support correctly rejecting lures regardless of their semantic/perceptual characteristics. Direct comparisons between related and unrelated correct rejections showed that unrelated correct rejections were associated with greater activity in bilateral middle and inferior temporal cortices, regions that have been associated with categorical processing and semantic labels. Related correct rejections showed greater activation in visual and lateral prefrontal cortices, which have been associated with perceptual processing and retrieval monitoring. Thus, while related and unrelated correct rejections show some common neural correlates, related correct rejections are driven by greater perceptual processing whereas unrelated correct rejections show greater reliance on salient categorical cues to support quick and accurate memory decisions.

Abstract memory representations in the ventromedial prefrontal cortex and hippocampus support concept generalization

Memory function involves both the ability to remember details of individual experiences and the ability to link information across events to create new knowledge. Prior research has identified the ventromedial prefrontal cortex (VMPFC) and the hippocampus as important for integrating across events in the service of generalization in episodic memory. The degree to which these memory integration mechanisms contribute to other forms of generalization, such as concept learning, is unclear. The present study used a concept-learning task in humans (both sexes) coupled with model-based fMRI to test whether VMPFC and hippocampus contribute to concept generalization, and whether they do so by maintaining specific category exemplars or abstract category representations. Two formal categorization models were fit to individual subject data: a prototype model that posits abstract category representations and an exemplar model that posits category representations based on individual category members. Latent variables from each of these models were entered into neuroimaging analyses to determine whether VMPFC and the hippocampus track prototype or exemplar information during concept generalization. Behavioral model fits indicated that almost three-quarters of the subjects relied on prototype information when making judgments about new category members. Paralleling prototype dominance in behavior, correlates of the prototype model were identified in VMPFC and the anterior hippocampus with no significant exemplar correlates. These results indicate that the VMPFC and portions of the hippocampus play a broad role in memory generalization and that they do so by representing abstract information integrated from multiple events. SIGNIFICANCE STATEMENT Whether people represent concepts as a set of individual category members or by deriving generalized concept representations abstracted across exemplars has been debated. In episodic memory, generalized memory representations have been shown to arise through integration across events supported by the ventromedial prefrontal cortex (VMPFC) and hippocampus. The current study combined formal categorization models with fMRI data analysis to show that the VMPFC and anterior hippocampus represent abstract prototype information during concept generalization, contributing novel evidence of generalized concept representations in the brain. Results indicate that VMPFC–hippocampal memory integration mechanisms contribute to knowledge generalization across multiple cognitive domains, with the degree of abstraction of memory representations varying along the long axis of the hippocampus.

Repeated study of items with and without repeated context: aging effects on memory discriminability

ABSTRACT Presenting items multiple times during encoding is a common way to enhance recognition accuracy. Under such conditions, older adults often show an increase in false recognition that counteracts benefits of repeated study. Using a false-memory paradigm with related study items and related lures, we tested whether repetition within the same encoding task or repetition across two different encoding tasks would be more beneficial to older adults’ memory discriminability. Results showed that, compared to items not repeated at study, items repeated in the same context and items repeated across different contexts showed improvements in memory discriminability in both young and older adults. This improvement was primarily reflected in improved recollection responses for both age groups across both repeat study conditions, as compared to no repetition. Importantly, the results demonstrated that repetition can be used to successfully mitigate age-related deficits by increasing memory discriminability and without incurring a cost of false recognition specific to any one age group.

Modulation of Target Recollection and Recollection Rejection Networks Due to Retrieval Facilitation and Interference.

To better understand neural recollection processing, we induced interference in target recollection by presenting related lures before their respective targets and facilitated recollection rejection of lures by presenting targets before their related lures. Target recollection following interference recruited visual and prefrontal cortices, showing that these regions support recollection when related information has disrupted target representations. Recollection rejection following target presentation recruited angular gyrus, indicating that this region supports recollection rejection when target representations are strong and highly accessible. Thus, recollection networks are sensitive to the accessibility of target representations that are affected by the presentation of related information during retrieval.