Brain mechanisms of successful recognition through retrieval of semantic context

Episodic memory is associated with the encoding and retrieval of context information and with a subjective sense of reexperiencing past events. The neural correlates of episodic retrieval have been extensively studied using fMRI, leading to the identification of a "general recollection network" including medial temporal, parietal, and prefrontal regions. However, in these studies, it is difficult to disentangle the effects of context retrieval from recollection. In this study, we used fMRI to determine the extent to which the recruitment of regions in the recollection network is contingent on context reinstatement. Participants were scanned during a cued recognition test for target words from encoded sentences. Studied target words were preceded by either a cue word studied in the same sentence (thus congruent with encoding context) or a cue word studied in a different sentence (thus incongruent with encoding context). Converging fMRI results from independently defined ROIs and whole-brain analysis showed regional specificity in the recollection network. Activity in hippocampus and parahippocampal cortex was specifically increased during successful retrieval following congruent context cues, whereas parietal and prefrontal components of the general recollection network were associated with confident retrieval irrespective of contextual congruency. Our findings implicate medial temporal regions in the retrieval of semantic context, contributing to, but dissociable from, recollective experience

Neural oscillations during conditional associative learning.

Associative learning requires mapping between complex stimuli and behavioural responses. When multiple stimuli are involved, conditional associative learning is a gradual process with learning based on trial and error. It is established that a distributed network of regions track associative learning, however the role of neural oscillations in human learning remains less clear. Here we used scalp EEG to test how neural oscillations change during learning of arbitrary visuo-motor associations. Participants learned to associative 48 different abstract shapes to one of four button responses through trial and error over repetitions of the shapes. To quantify how well the associations were learned for each trial, we used a state-space computational model of learning that provided a probability of each trial being correct given past performance for that stimulus, that we take as a measure of the strength of the association. We used linear modelling to relate single-trial neural oscillations to single-trial measures of association strength. We found frontal midline theta oscillations during the delay period tracked learning, where theta activity was strongest during the early stages of learning and declined as the associations were formed. Further, posterior alpha and low-beta oscillations in the cue period showed strong desynchronised activity early in learning, while stronger alpha activity during the delay period was seen as associations became well learned. Moreover, the magnitude of these effects during early learning, before the associations were learned, related to improvements in memory seen on the next presentation of the stimulus. The current study provides clear evidence that frontal theta and posterior alpha/beta oscillations play a key role during associative memory formation

Adaptive task difficulty influences neural plasticity and transfer of training

The efficacy of cognitive training is controversial, and research progress in the field requires an understanding of factors that promote transfer of training gains and their relationship to changes in brain activity. One such factor may be adaptive task difficulty, as adaptivity is predicted to facilitate more efficient processing by creating a prolonged mismatch between the supply of, and the demand upon, neural resources. To test this hypothesis, we measured behavioral and neural plasticity in fMRI sessions before and after 10 sessions of working memory updating (WMU) training, in which the difficulty of practiced tasks either adaptively increased in response to performance or was fixed. Adaptive training resulted in transfer to an untrained episodic memory task and activation decreases in striatum and hippocampus on a trained WMU task, and the amount of training task improvement was associated with near transfer to other WMU tasks and with hippocampal activation changes on both near and far transfer tasks. These findings suggest that cognitive training programs should incorporate adaptive task difficulty to broaden transfer of training gains and maximize efficiency of task-related brain activity

States of curiosity modulate hippocampus-dependent learning via the dopaminergic circuit

People find it easier to learn about topics that interest them, but little is known about the mechanisms by which intrinsic motivational states affect learning. We used functional magnetic resonance imaging to investigate how curiosity (intrinsic motivation to learn) influences memory. In both immediate and one-day-delayed memory tests, participants showed improved memory for information that they were curious about and for incidental material learned during states of high curiosity. Functional magnetic resonance imaging results revealed that activity in the midbrain and the nucleus accumbens was enhanced during states of high curiosity. Importantly, individual variability in curiosity-driven memory benefits for incidental material was supported by anticipatory activity in the midbrain and hippocampus and by functional connectivity between these regions. These findings suggest a link between the mechanisms supporting extrinsic reward motivation and intrinsic curiosity and highlight the importance of stimulating curiosity to create more effective learning experiences

How curiosity enhances hippocampus-dependent memory: The Prediction,Appraisal,Curiosity, Exploration (PACE) Framework

Curiosity plays a fundamental role for learning and memory, but the neural mechanisms that stimulate curiosity and its effect on memory are poorly understood. Accumulating evidence suggests that curiosity states are related to modulations in activity in the dopaminergic circuit and that these modulations impact memory encoding and consolidation for both targets of curiosity and incidental information encountered during curiosity states. To account for this evidence, we propose the Prediction, Appraisal, Curiosity, and Exploration (PACE) framework, which attempts to explain curiosity and memory in terms of cognitive processes, neural circuits, behavior, and subjective experience. The PACE framework generates testable predictions that can stimulate future investigation of the mechanisms underlying curiosity-related memory enhancements

Learning Warps Object Representations in the Ventral Temporal Cortex.

The human ventral temporal cortex (VTC) plays a critical role in object recognition. Although it is well established that visual experience shapes VTC object representations, the impact of semantic and contextual learning is unclear. In this study, we tracked changes in representations of novel visual objects that emerged after learning meaningful information about each object. Over multiple training sessions, participants learned to associate semantic features (e.g., "made of wood," "floats") and spatial contextual associations (e.g., "found in gardens") with novel objects. fMRI was used to examine VTC activity for objects before and after learning. Multivariate pattern similarity analyses revealed that, after learning, VTC activity patterns carried information about the learned contextual associations of the objects, such that objects with contextual associations exhibited higher pattern similarity after learning. Furthermore, these learning-induced increases in pattern information about contextual associations were correlated with reductions in pattern information about the object's visual features. In a second experiment, we validated that these contextual effects translated to real-life objects. Our findings demonstrate that visual object representations in VTC are shaped by the knowledge we have about objects and show that object representations can flexibly adapt as a consequence of learning with the changes related to the specific kind of newly acquired information.This project has received funding to LKT from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No 669820), from the European Research Council under the European Community's Seventh Framework Programme (FP7/2007 - 2013)/ERC Grant agreement n° 249640, and a Guggenheim Fellowship to CR.This is the final version of the article. It first appeared from MIT Press via http://dx.doi.org/10.1162/jocn_a_0095

Theta oscillations promote temporal sequence learning.

Many theoretical models suggest that neural oscillations play a role in learning or retrieval of temporal sequences, but the extent to which oscillations support sequence representation remains unclear. To address this question, we used scalp electroencephalography (EEG) to examine oscillatory activity over learning of different object sequences. Participants made semantic decisions on each object as they were presented in a continuous stream. For three "Consistent" sequences, the order of the objects was always fixed. Activity during Consistent sequences was compared to "Random" sequences that consisted of the same objects presented in a different order on each repetition. Over the course of learning, participants made faster semantic decisions to objects in Consistent, as compared to objects in Random sequences. Thus, participants were able to use sequence knowledge to predict upcoming items in Consistent sequences. EEG analyses revealed decreased oscillatory power in the theta (4-7 Hz) band at frontal sites following decisions about objects in Consistent sequences, as compared with objects in Random sequences. The theta power difference between Consistent and Random only emerged in the second half of the task, as participants were more effectively able to predict items in Consistent sequences. Moreover, we found increases in parieto-occipital alpha (10-13 Hz) and beta (14-28 Hz) power during the pre-response period for objects in Consistent sequences, relative to objects in Random sequences. Linear mixed effects modeling revealed that single trial theta oscillations were related to reaction time for future objects in a sequence, whereas beta and alpha oscillations were only predictive of reaction time on the current trial. These results indicate that theta and alpha/beta activity preferentially relate to future and current events, respectively. More generally our findings highlight the importance of band-specific neural oscillations in the learning of temporal order information.This work was supported by a Vannevar Bush Fellowship (Office of Naval Research Grant N00014-15-1-0033) and a Multi-University Research Initiative Grant (Office of Naval Research Grant N00014-17-1-2961) from the Office of Naval Research

Entrainment enhances theta oscillations and improves episodic memory.

Neural oscillations in the theta band have been linked to episodic memory, but it is unclear whether activity patterns that give rise to theta play a causal role in episodic retrieval. Here, we used rhythmic auditory and visual stimulation to entrain neural oscillations to assess whether theta activity contributes to successful memory retrieval. In two separate experiments, human subjects studied words and were subsequently tested on memory for the words ('item recognition') and the context in which each had been previously studied ('source memory'). Between study and test, subjects in the entrainment groups were exposed to audiovisual stimuli designed to enhance activity at 5.5 Hz, whereas subjects in the control groups were exposed to white noise (Expt. 1) or 14 Hz entrainment (Expt. 2). Theta entrainment selectively increased source memory performance in both studies. Electroencephalography (EEG) data in Expt. 2 revealed that theta entrainment resulted in band-specific enhancement of theta power during the entrainment period and during post-entrainment memory retrieval. These results demonstrate a direct link between theta activity and episodic memory retrieval. Targeted manipulation of theta activity could be a promising new approach to enhance theta activity and memory performance in healthy individuals and in patients with memory disorders

Hippocampal activity patterns carry information about objects in temporal context

The hippocampus is critical for human episodic memory, but its role remains controversial. One fundamental question concerns whether the hippocampus represents specific objects or assigns context-dependent representations to objects. Here, we used multivoxel pattern similarity analysis of fMRI data during retrieval of learned object sequences to systematically investigate hippocampal coding of object and temporal context information. Hippocampal activity patterns carried information about the temporal positions of objects in learned sequences, but not about objects or temporal positions in random sequences. Hippocampal activity patterns differentiated between overlapping object sequences and between temporally adjacent objects that belonged to distinct sequence contexts. Parahippocampal and perirhinal cortex showed different pattern information profiles consistent with coding of temporal position and object information, respectively. These findings are consistent with models proposing that the hippocampus represents objects within specific temporal contexts, a capability that might explain its critical role in episodic memory

Post-learning hippocampal dynamics promote preferential retention of rewarding events

Reward motivation is known to modulate memory encoding, and this effect depends on interactions between the substantia nigra/ventral tegmental area complex (SN/VTA) and the hippocampus. It is unknown, however, whether these interactions influence offline neural activity in the human brain that is thought to promote memory consolidation. Here we used fMRI to test the effect of reward motivation on post-learning neural dynamics and subsequent memory for objects that were learned in high- and low-reward motivation contexts. We found that post-learning increases in resting-state functional connectivity between the SN/VTA and hippocampus predicted preferential retention of objects that were learned in high-reward contexts. In addition, multivariate pattern classification revealed that hippocampal representations of high-reward contexts were preferentially reactivated during post-learning rest, and the number of hippocampal reactivations was predictive of preferential retention of items learned in high-reward contexts. These findings indicate that reward motivation alters offline post-learning dynamics between the SN/VTA and hippocampus, providing novel evidence for a potential mechanism by which reward could influence memory consolidatio