Dagmar Zeithamova

Dual-task interference in perceptual category learning

The effect of a working-memory—demanding dual task on perceptual category learning was investigated. In Experiment 1, participants learned unidimensional rule-based or information integration category structures. In Experiment 2, participants learned a conjunctive rule-based category structure. In Experiment 1, unidimensional rule-based category learning was disrupted more by the dual working memory task than was information integration category learning. In addition, rule-based category learning differed qualitatively from information integration category learning in yielding a bimodal, rather than a normal, distribution of scores. Experiment 2 showed that rule-based learning can be disrupted by a dual working memory task even when both dimensions are relevant for optimal categorization. The results support the notion of at least two systems of category learning: a hypothesis-testing system that seeks verbalizable rules and relies on working memory and selective attention, and an implicit system that is procedural-learning based and is essentially automatic.

The hippocampus and inferential reasoning: building memories to navigate future decisions

A critical aspect of inferential reasoning is the ability to form relationships between items or events that were not experienced together. This review considers different perspectives on the role of the hippocampus in successful inferential reasoning during both memory encoding and retrieval. Intuitively, inference can be thought of as a logical process by which elements of individual existing memories are retrieved and recombined to answer novel questions. Such flexible retrieval is sub-served by the hippocampus and is thought to require specialized hippocampal encoding mechanisms that discretely code events such that event elements are individually accessible from memory. In addition to retrieval-based inference, recent research has also focused on hippocampal processes that support the combination of information acquired across multiple experiences during encoding. This mechanism suggests that by recalling past events during new experiences, connections can be created between newly formed and existing memories. Such hippocampally mediated memory integration would thus underlie the formation of networks of related memories that extend beyond direct experience to anticipate future judgments about the relationships between items and events. We also discuss integrative encoding in the context of emerging evidence linking the hippocampus to the formation of schemas as well as prospective theories of hippocampal function that suggest memories are actively constructed to anticipate future decisions and actions.

Flexible Memories: Differential Roles for Medial Temporal Lobe and Prefrontal Cortex in Cross-Episode Binding

Episodic memory is characterized by rapid formation of new associations that bind information within individual episodes. A powerful aspect of episodic memory is the ability to flexibly apply and recombine information from past experience to guide new behavior. A critical question for memory research is how medial temporal lobe (MTL) and prefrontal cortex (PFC), regions implicated in rapid within-episode binding, further support cross-episode binding in service of mnemonic flexibility. We set to answer this question using an associative inference task in humans that required rapid binding of information across overlapping experiences (AB, BC) to enable successful transfer to novel test probes (AC). Within regions predicting subsequent associative memory for directly learned associations, encoding activation in MTL, including hippocampus and parahippocampal cortex, uniquely predicted success on novel transfer trials both within and across participants, consistent with an integrative encoding mechanism where overlapping experiences are linked into a combined representation during learning. In contrast, during retrieval, PFC activation predicted trial-by-trial transfer success while MTL predicted transfer performance across participants. Moreover, increased MTL-PFC coupling was observed during novel transfer trials compared with retrieval of directly learned associations. These findings suggest that inferential processes support transfer of rapidly acquired experiences to novel events during retrieval where multiple memories are recalled and flexibly recombined in service of successful behavior. Together, these results demonstrate distinct encoding and retrieval mechanisms that support mnemonic flexibility, revealing a unique role for MTL regions in cross-episode binding during encoding and engagement of interactive MTL-PFC processes during flexible transfer at test.

Dissociable Prototype Learning Systems: Evidence from Brain Imaging and Behavior

The neural underpinnings of prototype learning are not well understood. A major source of confusion is that two versions of the prototype learning task have been used interchangeably in the literature; one where participants learn to categorize exemplars derived from two prototypes (A/B task), and one where participants learn to categorize exemplars derived from one prototype and noncategorical exemplars (A/non-A). We report results from an fMRI study of A/B and A/non-A prototype learning that allows for a direct contrast of the two learning methods. Accuracy in the two tasks did not correlate within subject despite equivalent average difficulty. The fMRI results revealed neural activation in a network of regions consistent with episodic memory retrieval for the A/B task while greater activation of a nondeclarative learning network was observed for the A/non-A task. The results demonstrate that learning in these two tasks is mediated by different neural systems and that recruitment of each system is dictated by the context of learning rather than the actual category structure.

The role of visuospatial and verbal working memory in perceptual category learning

The role of verbal and visuospatial working memory in rule-based and information-integration category learning was examined. Previously, Maddox, Ashby, Ing, and Pickering (2004) found that a sequentially presented verbal working memory task did not affect information-integration learning, but disrupted rule-based learning when the rule was on the spatial frequency of a Gabor stimulus. This pattern was replicated in Experiment 1, in which the same category structures were used, but in which the verbal working memory task was replaced with a visuospatial analog. Experiment 2A examined rule-based learning on an oblique orientation and also found both verbal and visuospatial working memory tasks disrupting learning. Experiment 2B examined rule-based learning on a cardinal orientation and found a minimal effect of the verbal working memory task, but a large effect of the visuospatial working memory task. The conceptual significance of cardinal orientations and the role of visuospatial and verbal working memory in category learning are discussed.

Reward modulation of hippocampal subfield activation during successful associative encoding and retrieval

Emerging evidence suggests that motivation enhances episodic memory formation through interactions between medial-temporal lobe (MTL) structures and dopaminergic midbrain. In addition, recent theories propose that motivation specifically facilitates hippocampal associative binding processes, resulting in more detailed memories that are readily reinstated from partial input. Here, we used high-resolution fMRI to determine how motivation influences associative encoding and retrieval processes within human MTL subregions and dopaminergic midbrain. Participants intentionally encoded object associations under varying conditions of reward and performed a retrieval task during which studied associations were cued from partial input. Behaviorally, cued recall performance was superior for high-value relative to low-value associations; however, participants differed in the degree to which rewards influenced memory. The magnitude of behavioral reward modulation was associated with reward-related activation changes in dentate gyrus/CA2,3 during encoding and enhanced functional connectivity between dentate gyrus/CA2,3 and dopaminergic midbrain during both the encoding and retrieval phases of the task. These findings suggests that, within the hippocampus, reward-based motivation specifically enhances dentate gyrus/CA2,3 associative encoding mechanisms through interactions with dopaminergic midbrain. Furthermore, within parahippocampal cortex and dopaminergic midbrain regions, activation associated with successful memory formation was modulated by reward across the group. During the retrieval phase, we also observed enhanced activation in hippocampus and dopaminergic midbrain for high-value associations that occurred in the absence of any explicit cues to reward. Collectively, these findings shed light on fundamental mechanisms through which reward impacts associative memory formation and retrieval through facilitation of MTL and ventral tegmental area/substantia nigra processing.

CA1 subfield contributions to memory integration and inference

The ability to combine information acquired at different times to make novel inferences is a powerful function of episodic memory. One perspective suggests that by retrieving related knowledge during new experiences, existing memories can be linked to the new, overlapping information as it is encoded. The resulting memory traces would thus incorporate content across event boundaries, representing important relationships among items encountered during separate experiences. While prior work suggests that the hippocampus is involved in linking memories experienced at different times, the involvement of specific subfields in this process remains unknown. Using both univariate and multivariate analyses of high‐resolution functional magnetic resonance imaging (fMRI) data, we localized this specialized encoding mechanism to human CA1. Specifically, right CA1 responses during encoding of events that overlapped with prior experience predicted subsequent success on a test requiring inferences about the relationships among events. Furthermore, we employed neural pattern similarity analysis to show that patterns of activation evoked during overlapping event encoding were later reinstated in CA1 during successful inference. The reinstatement of CA1 patterns during inference was specific to those trials that were performed quickly and accurately, consistent with the notion that linking memories during learning facilitates novel judgments. These analyses provide converging evidence that CA1 plays a unique role in encoding overlapping events and highlight the dynamic interactions between hippocampal‐mediated encoding and retrieval processes. More broadly, our data reflect the adaptive nature of episodic memories, in which representations are derived across events in anticipation of future judgments.

Distributed hippocampal patterns that discriminate reward context are associated with enhanced associative binding

Recent research indicates that reward-based motivation impacts medial temporal lobe (MTL) encoding processes, leading to enhanced memory for rewarded events. In particular, previous functional magnetic resonance imaging (fMRI) studies of motivated learning have shown that MTL activation is greater for highly rewarded events, with the degree of reward-related activation enhancement tracking the corresponding behavioral memory advantage. These studies, however, do not directly address leading theoretical perspectives that propose such reward-based enhancements in MTL encoding activation reflect enhanced discrimination of the motivational context of specific events. In this study, a high-value or low-value monetary cue preceded a pair of objects, indicating the future reward for successfully remembering the pair. Using representational similarity analysis and high-resolution fMRI, we show that MTL activation patterns are more similar for encoding trials preceded by the same versus different reward cues, indicating a distributed code in this region that distinguishes between motivational contexts. Moreover, we show that activation patterns in hippocampus and parahippocampal cortex (PHc) that differentiate reward conditions during anticipatory cues and object pairs relate to successful associative memory. Additionally, the degree to which patterns differentiate reward contexts in dentate gyrus/CA2,3 and PHc is related to individual differences in reward modulation of memory. Collectively, these findings suggest that distributed activation patterns in the human hippocampus and PHc reflect the rewards associated with individual events. Furthermore, we show that these activation patterns-which discriminate between reward conditions--may influence memory through the incorporation of information about motivational contexts into stored memory representations.

Learning mode and exemplar sequencing in unsupervised category learning

Exemplar sequencing effects in incidental and intentional unsupervised category learning were investigated to illuminate how people form categories without an external teacher. Stimuli were perfectly separable into 2 categories based on 1 of 2 dimensions of variation. Sequencing of the first 20 training stimuli was manipulated. In the blocked condition, 10 Category A stimuli were followed by 10 Category B stimuli. In the intermixed condition, these 20 stimuli were ordered randomly. Experiment 1 revealed an interaction between learning mode and sequence, with better intentional learning for intermixed sequences but better incidental learning for blocked sequences. Experiment 2 showed that manipulating trial-to-trial variability along each dimension can impact intentional learning. Training sequences that emphasized variation along the category-relevant dimension resulted in better performance than sequences that emphasized variation along the category-irrelevant dimension. The results suggest that unsupervised category learning is influenced by the mode of learning and the order and nature of encountered exemplars.

Temporal Proximity Promotes Integration of Overlapping Events

Events with overlapping elements can be encoded as two separate representations or linked into an integrated representation, yet we know little about the conditions that promote one form of representation over the other. Here, we tested the hypothesis that the proximity of overlapping events would increase the probability of integration. Participants first established memories for house–object and face–object pairs; half of the pairs were learned 24 hr before an fMRI session, and the other half 30 min before the session. During scanning, participants encoded object–object pairs that overlapped with the initial pairs acquired on the same or prior day. Participants were also scanned as they made inference judgments about the relationships among overlapping pairs learned on the same or different day. Participants were more accurate and faster when inferring relationships among memories learned on the same day relative to those acquired across days, suggesting that temporal proximity promotes integration. Evidence for reactivation of existing memories—as measured by a visual content classifier—was equivalent during encoding of overlapping pairs from the two temporal conditions. In contrast, evidence for integration—as measured by a mnemonic strategy classifier from an independent study [Richter, F. R., Chanales, A. J. H., & Kuhl, B. A. Predicting the integration of overlapping memories by decoding mnemonic processing states during learning. Neuroimage, 124, 323–335, 2016]—was greater for same-day overlapping events, paralleling the behavioral results. During inference itself, activation patterns further differentiated when participants were making inferences about events acquired on the same day versus across days. These findings indicate that temporal proximity of events promotes integration and further influences the neural mechanisms engaged during inference.