Brain structure and episodic learning rate in cognitively healthy ageing.

Memory normally declines with ageing and these age-related cognitive changes are associated with changes in brain structure. Episodic memory retrieval has been widely studied during ageing, whereas learning has received less attention. Here we examined the neural correlates of episodic learning rate in ageing. Our study sample consisted of 982 cognitively healthy female and male older participants from the Vallecas Project cohort, without a clinical diagnosis of mild cognitive impairment or dementia. The learning rate across the three consecutive recall trials of the verbal memory task (Free and Cued Selective Reminding Test) recall trials was used as a predictor of grey matter (GM) using voxel-based morphometry, and WM microstructure using tract-based spatial statistics on fractional anisotropy (FA) and mean diffusivity (MD) measures. Immediate Recall improved by 1.4 items per trial on average, and this episodic learning rate was faster in women and negatively associated with age. Structurally, hippocampal and anterior thalamic GM volume correlated positively with learning rate. Learning also correlated with the integrity of WM microstructure (high FA and low MD) in an extensive network of tracts including bilateral anterior thalamic radiation, fornix, and long-range tracts. These results suggest that episodic learning rate is associated with key anatomical structures for memory functioning, motivating further exploration of the differential diagnostic properties between episodic learning rate and retrieval in ageing.

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.

Pattern Separation Underpins Expectation-Modulated Memory.

Pattern separation and completion are fundamental hippocampal computations supporting memory encoding and retrieval. However, despite extensive exploration of these processes, it remains unclear whether and how top-down processes adaptively modulate the dynamics between these computations. Here we examine the role of expectation in shifting the hippocampus to perform pattern separation. In a behavioral task, 29 participants (7 males) learned a cue-object category contingency. Then, at encoding, one-third of the cues preceding the to-be-memorized objects, violated the studied rule. At test, participants performed a recognition task with old objects (targets) and a set of parametrically manipulated (very similar to dissimilar) foils for each object. Accuracy was found to be better for foils of high similarity to targets that were contextually unexpected at encoding compared with expected ones. Critically, there were no expectation-driven differences for targets and low similarity foils. To further explore these effects, we implemented a computational model of the hippocampus, performing the same task as the human participants. We used representational similarity analysis to examine how top-down expectation interacts with bottom-up perceptual input, in each layer. All subfields showed more dissimilar representations for unexpected items, with dentate gyrus (DG) and CA3 being more sensitive to expectation violation than CA1. Again, representational differences between expected and unexpected inputs were prominent for moderate to high levels of input similarity. This effect diminished when inputs from DG and CA3 into CA1 were lesioned. Overall, these novel findings strongly suggest that pattern separation in DG/CA3 underlies the effect that violation of expectation exerts on memory.SIGNIFICANCE STATEMENT What makes some events more memorable than others is a key question in cognitive neuroscience. Violation of expectation often leads to better memory performance, but the neural mechanism underlying this benefit remains elusive. In a behavioral study, we found that memory accuracy is enhanced selectively for unexpected highly similar foils, suggesting expectation violation does not enhance memory indiscriminately, but specifically aids the disambiguation of overlapping inputs. This is further supported by our subsequent investigation using a hippocampal computational model, revealing increased representational dissimilarity for unexpected highly similar foils in DG and CA3. These convergent results provide the first evidence that pattern separation plays an explicit role in supporting memory for unexpected information.

SOLID-Similar object and lure image database.

Stimulus selection is a critical part of experimental designs in the cognitive sciences. Quantifying and controlling item similarity using a unified scale provides researchers with the tools to eliminate item-dependent effects and improve reproducibility. Here we present a novel Similar Object and Lure Image Database (SOLID) that includes 201 categories of grayscale objects, with approximately 17 exemplars per set. Unlike existing databases, SOLID offers both a large number of stimuli and a considerable range of similarity levels. A common scale of dissimilarity was obtained by using the spatial-arrangement method (Exps. 1a and 1b) as well as a pairwise rating procedure to standardize the distances (Exp. 2). These dissimilarity distances were then validated in a recognition memory task, showing better performance and decreased response times as dissimilarity increased. These methods were used to produce a large stimulus database (3,498 images) with a wide range of comparable similarities, which will be useful for improving experimental control in fields such as memory, perception, and attention. Enabling this degree of control over similarity is critical for high-level studies of memory and cognition, and combining this strength with the option to use it across many trials will allow research questions to be addressed using neuroimaging techniques.

Beneficial and detrimental effects of schema incongruence on memory for contextual events.

Mental schemas provide a framework into which new information can easily be integrated. In a series of experiments, we examined how incongruence that stems from a prediction error modulates memory for multicomponent events that instantiated preexisting schemas as noted in a previous study. Each event consisted of four stimulus pairs with overlapping components, presented in four blocks (A-B, B-C, C-D, D-A). A-B pairs elicited contextual expectations (A: Farm, B: Tractor) that were either met by a congruent C component (C: Farmer) or violated by an incongruent one (C: Lawyer). The baseline condition included unrelated pairs, where the C component was neither congruent nor incongruent. In experiment 2, events were presented in successive trials instead of blocks, and eye movements were recorded to analyze allocation of attention. Memory was tested through old-new item recognition followed by cued recall. Across experiments, recognition and recall performance for incongruent components was reduced compared to congruent components. Incongruent items were in some cases more accurately retrieved compared to unrelated ones, depending on task demands. Additionally, better recall was observed in the incongruent D-A pairs, compared to congruent and unrelated ones, because of reduced interference from C components. Eye-tracking revealed an increased number of fixations on C components in the incongruent and unrelated conditions. These results suggest that the integration of incongruent items into an episode is impaired, compared to congruent items, despite the contextual surprise and increased attention they elicited at encoding. However, there was a beneficial effect of prediction error on memory performance, compared to a baseline, depending on the task used.

Insula and somatosensory cortical myelination and iron markers underlie individual differences in empathy.

Empathy is a key component of our ability to engage and interact with others. In recent years, the neural mechanisms underlying affective and cognitive empathy have garnered intense interest. This work demonstrates that empathy for others depends upon a distributed network of regions such as the insula, parietal cortex, and somatosensory areas, which are also activated when we ourselves experience an empathized-with emotion (e.g., pain). Individuals vary markedly in their ability to empathize with others, which predicts the tendency to help others and relates to individual differences in the neuroanatomy of these areas. Here, we use a newly developed, high-resolution (800 µm isotropic), quantitative MRI technique to better elucidate the neuroanatomical underpinnings of individual differences in empathy. Our findings extend previous studies of the neuroanatomical correlates of cognitive and affective empathy. In particular, individual differences in cognitive empathy were associated with markers of myeloarchitectural integrity of the insular cortex, while affective empathy was predicted by a marker of iron content in second somatosensory cortex. These results indicate potential novel biomarkers of trait empathy, suggesting that microstructural features of an empathy and body-related network are crucial for understanding the mental and emotional states of others.

Metacognitive ability correlates with hippocampal and prefrontal microstructure.

The ability to introspectively evaluate our experiences to form accurate metacognitive beliefs, or insight, is an essential component of decision-making. Previous research suggests individuals vary substantially in their level of insight, and that this variation is related to brain volume and function, particularly in the anterior prefrontal cortex (aPFC). However, the neurobiological mechanisms underlying these effects are unclear, as qualitative, macroscopic measures such as brain volume can be related to a variety of microstructural features. Here we leverage a high-resolution (800µm isotropic) multi-parameter mapping technique in 48 healthy individuals to delineate quantitative markers of in vivo histological features underlying metacognitive ability. Specifically, we examined how neuroimaging markers of local grey matter myelination and iron content relate to insight as measured by a signal-theoretic model of subjective confidence. Our results revealed a pattern of microstructural correlates of perceptual metacognition in the aPFC, precuneus, hippocampus, and visual cortices. In particular, we extend previous volumetric findings to show that right aPFC myeloarchitecture positively relates to metacognitive insight. In contrast, decreased myelination in the left hippocampus correlated with better metacognitive insight. These results highlight the ability of quantitative neuroimaging to reveal novel brain-behaviour correlates and may motivate future research on their environmental and developmental underpinnings.

Unexpected arousal modulates the influence of sensory noise on confidence.

Human perception is invariably accompanied by a graded feeling of confidence that guides metacognitive awareness and decision-making. It is often assumed that this arises solely from the feed-forward encoding of the strength or precision of sensory inputs. In contrast, interoceptive inference models suggest that confidence reflects a weighted integration of sensory precision and expectations about internal states, such as arousal. Here we test this hypothesis using a novel psychophysical paradigm, in which unseen disgust-cues induced unexpected, unconscious arousal just before participants discriminated motion signals of variable precision. Across measures of perceptual bias, uncertainty, and physiological arousal we found that arousing disgust cues modulated the encoding of sensory noise. Furthermore, the degree to which trial-by-trial pupil fluctuations encoded this nonlinear interaction correlated with trial level confidence. Our results suggest that unexpected arousal regulates perceptual precision, such that subjective confidence reflects the integration of both external sensory and internal, embodied states.