The hippocampus supports the representation of abstract concepts: Implications for the study of recognition memory.

Words, unlike images, are symbolic representations. The associative details inherent within a word's meaning and the visual imagery it generates, are inextricably connected to the way words are processed and represented. It is well recognised that the hippocampus associatively binds components of a memory to form a lasting representation, and here we show that the hippocampus is especially sensitive to abstract word processing. Using fMRI during recognition, we found that the increased abstractness of words produced increased hippocampal activation regardless of memory outcome. Interestingly, word recollection produced hippocampal activation regardless of word content, while the parahippocampal cortex was sensitive to concreteness of word representations, regardless of memory outcome. We reason that the hippocampus has assumed a critical role in the representation of uncontextualized abstract word meaning, as its information-binding ability allows the retrieval of the semantic and visual associates that, when bound together, generate the abstract concept represented by word symbols. These insights have implications for research on word representation, memory, and hippocampal function, perhaps shedding light on how the human brain has adapted to encode and represent abstract concepts.

Pupil response patterns distinguish true from false memories.

Memory is reconstructive and error-prone, which make memory illusions very common in everyday life. However, studying memory illusions can provide valuable insights into how memory works. Pupil response has emerged, in recent years, as an indicator of memory encoding and retrieval, however its validity as a measure of memory success is debated. In this study, we explored whether pupil response patterns can differentiate true from false memories and whether variations in the temporal dynamics of pupil response can elucidate the mechanisms underlying false memory creation. The Deese-Roediger-McDermott (DRM) paradigm was employed to generate false memories in two separate experiments involving visual and auditory stimuli. Pupil responses effectively differentiated true from false memories based on variations in pupil amplitude at different temporal components. This discrimination remained consistent across both experiments, with slightly stronger effects in the auditory condition, aligning with the more pronounced false memory effects in this condition. Notably, differential pupil responses between true and false memories varied based on the type of memory involved at recognition. These findings provide valuable insights into the cognitive processes underlying memory distortions, with implications for theoretical frameworks and real-world contexts.

Experiencing Surprise: The Temporal Dynamics of Its Impact on Memory.

To efficiently process information, the brain shifts between encoding and retrieval states, prioritizing bottom-up or top-down processing accordingly. Expectation violation before or during learning has been shown to trigger an adaptive encoding mechanism, resulting in better memory for unexpected events. Using fMRI, we explored (1) whether this encoding mechanism is also triggered during retrieval, and if so, (2) what the temporal dynamics of its mnemonic consequences are. Male and female participants studied object images, then, with new objects, they learned a contingency between a cue and a semantic category. Rule-abiding (expected) and violating (unexpected) targets and similar foils were used at test. We found interactions between previous and current similar events' expectation, such that when an expected event followed a similar but unexpected event, its performance was boosted, underpinned by activation in the hippocampus, midbrain, and occipital cortex. In contrast, a sequence of two unexpected similar events also triggered occipital engagement; however, this did not enhance memory performance. Taken together, our findings suggest that when the goal is to retrieve, encountering surprising events engages an encoding mechanism, supported by bottom-up processing, that may enhance memory for future related events.SIGNIFICANCE STATEMENT Optimizing the balance between new learning and the retrieval of existing knowledge is an ongoing process, at the core of human cognition. Previous research into memory encoding suggests experiencing surprise leads to the prioritization of the learning of new memories, forming an adaptive encoding mechanism. We examined whether this mechanism is also engaged when the current goal is to retrieve information. Our results demonstrate that an expectation-driven shift toward an encoding state, supported by enhanced perceptual processing, is beneficial for the correct identification of subsequent expected similar events. These findings have important implications for our understanding of the temporal dynamics of the adaptive encoding of information into memory.

Expectation-driven novelty effects in episodic memory.

Novel and unexpected stimuli are often prioritised in memory, given their inherent salience. Nevertheless, not all forms of novelty show such an enhancement effect. Here, we discuss the role expectation plays in modulating the way novelty affects memory processes, circuits, and subsequent performance. We first review independent effects of expectation on memory, and then consider how different types of novelty are characterised by expectation. We argue that different types of novelty defined by expectation implicate differential neurotransmission in memory formation brain regions and may also result in the creation of different types of memory. Contextual novelty, which is unexpected by definition, is often associated with better recollection, supported by dopaminergic-hippocampal interactions. On the other hand, expected stimulus novelty is supported by engagement of medial temporal cortices, as well as the hippocampus, through cholinergic modulation. Furthermore, when expected stimulus novelty results in enhanced memory, it is predominantly driven by familiarity. The literature reviewed here highlights the complexity of novelty-sensitive memory systems, the distinction between types of novelty, and how they are differentially affected by expectancy.

Encoding-linked pupil response is modulated by expected and unexpected novelty: Implications for memory formation and neurotransmission.

Whether a novel stimulus is expected or unexpected may have implications for the kind of ensuing encoding and the type of subsequent memory. Pupil response was used in the present study to explore the way expected and unexpected stimuli are encoded and whether encoding-linked pupil response is modulated by expectation. Participants first established a contingency relationship between a series of symbols and the type of stimulus (man-made or natural) that followed each one. At encoding, some of the target stimuli violated the previously established relationship (i.e., unexpected), while the majority conformed to this relationship (i.e., expected). Expectation at encoding had opposite effects on familiarity and recollection, the two types of memory that support recognition, and modulated differently the way pupil response predicted subsequent memory. Encoding of unexpected novel stimuli was associated with increased pupil dilation as a predictor of subsequent memory type and strength. In contrast, encoding of expected novel stimuli was associated with decreased pupil response (constriction), which was predictive of subsequent memory type and strength. The findings support the close link between pupil response and memory formation, but critically indicate that this is modulated by the type of novelty as defined by expectation. These novel findings have important implications for the encoding mechanisms involved when different types of novelty are detected and is proposed to indicate the operation of different neurotransmitters during memory formation.

Thalamic-Medial Temporal Lobe Connectivity Underpins Familiarity Memory.

The neural basis of memory is highly distributed, but the thalamus is known to play a particularly critical role. However, exactly how the different thalamic nuclei contribute to different kinds of memory is unclear. Moreover, whether thalamic connectivity with the medial temporal lobe (MTL), arguably the most fundamental memory structure, is critical for memory remains unknown. We explore these questions using an fMRI recognition memory paradigm that taps familiarity and recollection (i.e., the two types of memory that support recognition) for objects, faces, and scenes. We show that the mediodorsal thalamus (MDt) plays a material-general role in familiarity, while the anterior thalamus plays a material-general role in recollection. Material-specific regions were found for scene familiarity (ventral posteromedial and pulvinar thalamic nuclei) and face familiarity (left ventrolateral thalamus). Critically, increased functional connectivity between the MDt and the parahippocampal (PHC) and perirhinal cortices (PRC) of the MTL underpinned increases in reported familiarity confidence. These findings suggest that familiarity signals are generated through the dynamic interaction of functionally connected MTL-thalamic structures.

Amount, not strength of recollection, drives hippocampal activity: A problem for apparent word familiarity-related hippocampal activation.

The role of the hippocampus in recollection and familiarity remains debated. Using functional magnetic resonance imaging (fMRI), we explored whether hippocampal activity is modulated by increasing recollection confidence, increasing amount of recalled information, or both. We also investigated whether any hippocampal differences between recollection and familiarity relate to processing differences or amount of information in memory. Across two fMRI tasks, we separately compared brain responses to levels of confidence for cued word recall and word familiarity, respectively. Contrary to previous beliefs, increasing confidence/accuracy of cued recall of studied words did not increase hippocampal activity, when unconfounded by amount recollected. In contrast, additional recollection (i.e., recollecting more information than the word alone) increased hippocampal activity, although its accuracy matched that of word recall alone. Unlike cued word recall, increasing word familiarity accuracy did increase hippocampal activity linearly, although at an uncorrected level. This finding occurred although cued word recall and familiarity memory seemed matched with respect to information in memory. The detailed characteristics of these effects do not prove that word familiarity is exceptional in having hippocampal neural correlates. They suggest instead that participants fail to identify some aspects of recollection, misreporting it as familiarity, a problem with word-like items that have strong and recallable semantic associates.

Expectation affects learning and modulates memory experience at retrieval.

Our ability to make predictions and monitor regularities has a profound impact on the way we perceive the environment, but the effect this mechanism has on memory is not well understood. In four experiments, we explored the effects on memory of the expectation status of information at encoding or at retrieval. In a rule-learning task participants learned a contingency relationship between 6 different symbols and the type of stimulus that followed each one. Either at encoding (Experiments 1a and 1b) or at retrieval (Experiments 2a and 2b), the established relationship was violated for a subset of stimuli resulting in the presentation of both expected and unexpected stimuli. The expectation status of the stimuli was found to have opposite effects on familiarity and recollection performance, the two kinds of memory that support recognition memory. At encoding (Experiments 1a and 1b), the presentation of expected stimuli selectively enhanced subsequent familiarity performance, while unexpected stimuli selectively enhanced subsequent recollection. Similarly, at retrieval (Experiments 2a and 2b), expected stimuli were more likely to be deemed familiar than unexpected stimuli, whereas unexpected stimuli were more likely to be recollected than were expected stimuli. These findings suggest that two separate memory enhancement mechanisms exist; one sensitive and modulating the accuracy of memory for the contextually distinctive or unexpected, and the other sensitive to and modulating the accuracy of memory for the expected. Therefore, the degree to which information fits with expectation has critical implications for the type of computational mechanism that will be engaged to support memory.

How do memory systems detect and respond to novelty?

The efficiency of the memory system lies not only in its readiness to detect and retrieve old stimuli but also in its ability to detect and integrate novel information. In this review, we discuss recent evidence suggesting that the neural substrates sensitive to detecting familiarity and novelty are not entirely overlapping. Instead, these partially distinct familiarity and novelty signals are integrated to support recognition memory decisions. We propose here that the mediodorsal thalamus is critical for familiarity detection, and for combining novelty signals from the medial temporal lobe cortex with the relative familiarity outputs of computations performed in other cortical structures, especially the prefrontal cortex. Importantly, we argue that the anterior hippocampus has a prominent role in detecting novelty and in communicating this with midbrain and striatal structures. We argue that different types of novelty (absolute or contextual) engage different neurotransmitter systems that converge in the hippocampus. We suggest that contextual or unexpected novelty triggers dopaminergic hippocampal-midbrain coupling and noradrenergic-mediated pupil dilation. In contrast, absolute novelty triggers cholinergic-mediated hippocampal encoding accompanied by diminished pupil dilation. These two, distinct hippocampal encoding mechanisms both lead to later recollection but are sensitive to different types of novelty. We conclude that this neurotransmitter-mediated hippocampal encoding establishes the hippocampus in an encoding mode that briefly prevents the engagement of retrieval.

Material Specificity Drives Medial Temporal Lobe Familiarity But Not Hippocampal Recollection.

The specific role of the perirhinal (PRC), entorhinal (ERC) and parahippocampal cortices (PHC) in supporting familiarity-based recognition remains unknown. An fMRI study explored whether these medial temporal lobe (MTL) structures responded in the same way or differentially to familiarity as a function of stimulus type at recognition. A secondary aim was to explore whether the hippocampus responds in the same way to equally strong familiarity and recollection and whether this is influenced by the kind of stimulus involved. Univariate and multivariate analyses revealed that familiarity responses in the PRC, ERC, PHC and the amygdala are material-specific. Specifically, the PRC and ERC selectively responded to object familiarity, while the PHC responded to both object and scene familiarity. The amygdala only responded to familiarity memory for faces. The hippocampus did not respond to stimulus familiarity for any of the three types of stimuli, but it did respond to recollection for all three types of stimuli. This was true even when recollection was contrasted to equally accurate familiarity. Overall, the findings suggest that the role of the MTL neocortices and the amygdala in familiarity-based recognition depends on the kind of stimulus in memory, whereas the role of the hippocampus in recollection is independent of the type of cuing stimulus. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.