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Barry, D. N.

Publications and source records attributed to Barry, D. N..

6 recordsLinked to original sources

A neural network account of memory replay and knowledge consolidation

Replay can consolidate memories through offline neural reactivation related to past experiences. Category knowledge is learned across multiple experiences, and its subsequent generalisation is promoted by consolidation and replay during rest and sleep. However, aspects of replay are difficult to determine from neuroimaging studies. We provided insights into category knowledge replay by simulating these processes in a neural network which approximated the roles of the human ventral visual stream and hippocampus. Generative replay, akin to imagining new category instances, facilitated generalisation to new experiences. Consolidation-related replay may therefore help to prepare us for the future as much as remember the past. Generative replay was more effective in later network layers functionally similar to the lateral occipital cortex than layers corresponding to early visual cortex, drawing a distinction between neural replay and its relevance to consolidation. Category replay was most beneficial for newly acquired knowledge, suggesting replay helps us adapt to changes in our environment. Finally, we present a novel mechanism for the observation that the brain selectively consolidates weaker information; a reinforcement learning process in which categories were replayed according to their contribution to network performance. This reinforces the idea of consolidation-related replay as an active rather than passive process.

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Testing covariance models for MEG source reconstruction of hippocampal activity

Beamforming is one of the most commonly used source reconstruction methods for magneto- and electroencephalography (M/EEG). One underlying assumption, however, is that distant sources are uncorrelated and here we tested whether this is an appropriate model for the human hippocampal data. We revised the Empirical Bayesian Beamfomer (EBB) to accommodate specific a-priori correlated source models. We showed in simulation that we could use model evidence (as approximated by Free Energy) to distinguish between different correlated and uncorrelated source scenarios. Using group MEG data in which the participants performed a hippocampal-dependent task, we explored the possibility that the hippocampus or the cortex or both were correlated in their activity across hemispheres. We found that incorporating a correlated hippocampal source model significantly improved model evidence. Our findings help to explain why, up until now, the majority of MEG-reported hippocampal activity (typically making use of beamformers) has been estimated as unilateral.

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vmPFC drives hippocampal processing during autobiographical memory recall regardless of remoteness

Our ability to recall past experiences, autobiographical memories (AMs), is crucial to cognition, endowing us with a sense of self and underwriting our capacity for autonomy. Traditional views assume that the hippocampus orchestrates event recall, whereas recent accounts propose that the ventromedial prefrontal cortex (vmPFC) instigates and coordinates hippocampal-dependent processes. Here we sought to characterise the dynamic interplay between hippocampus and vmPFC during AM recall to adjudicate between these perspectives. Leveraging the high temporal resolution of magnetoencephalography, we found that the left hippocampus and the vmPFC showed the greatest power changes during AM retrieval. Moreover, responses in the vmPFC preceded activity in the hippocampus during initiation of AM recall, except during retrieval of the most recent AMs. The vmPFC drove hippocampal activity during recall initiation and also as AMs unfolded over subsequent seconds, and this effect was evident regardless of AM age. These results re-cast the positions of the hippocampus and the vmPFC in the AM retrieval hierarchy, with implications for theoretical accounts of memory processing and systems-level consolidation.

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Mouth magnetoencephalography: A unique perspective on the human hippocampus

Traditional magnetoencephalographic (MEG) brain imaging scanners consist of a rigid sensor array surrounding the head; this means that they are maximally sensitive to superficial brain structures. New technology based on optical pumping means that we can now consider more flexible and creative sensor placement. Here we explored the magnetic fields generated by a model of the human hippocampus not only across scalp but also at the roof of the mouth. We found that simulated hippocampal sources gave rise to dipolar field patterns with one scalp surface field extremum at the temporal lobe and a corresponding maximum or minimum at the roof of the mouth. We then constructed a fitted dental mould to accommodate an Optically Pumped Magnetometer (OPM). We collected data using a previously validated hippocampal-dependent task to test the empirical utility of a mouth-based sensor, with an accompanying array of left and right temporal lobe OPMs. We found that the mouth sensor showed the greatest task-related theta power change. We also found that, as predicted by the simulations, the mouth sensor was anti-correlated with those on over the temporal lobes. We found that this sensor had a mild effect on the reconstructed power in the hippocampus (~10% change) but that coherence images between the mouth sensor and reconstructed source images showed a global maximum in the right hippocampus. We conclude that augmenting a scalp-based MEG array with sensors in the mouth shows unique promise for both basic scientists and clinicians interested in interrogating the hippocampus.

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The neural dynamics of novel scene imagery

Retrieval of long-term episodic memories is characterised by synchronised neural activity between hippocampus and ventromedial prefrontal cortex (vmPFC), with additional evidence that vmPFC activity leads that of the hippocampus. It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. If this is the case, then a comparable interaction between the two brain regions should exist during the construction of novel scene imagery. To address this question, we leveraged the high temporal resolution of magnetoencephalography (MEG) to investigate the construction of novel mental imagery. We tasked male and female humans with imagining scenes and single isolated objects in response to one-word cues. We performed source level power, coherence and causality analyses to characterise the underlying inter-regional interactions. Both scene and object imagination resulted in theta power changes in the anterior hippocampus. However, higher theta coherence was observed between the hippocampus and vmPFC in the scene compared to the object condition. This inter-regional theta coherence also predicted whether or not imagined scenes were subsequently remembered. Dynamic causal modelling of this interaction revealed that vmPFC drove activity in hippocampus during novel scene construction. Additionally, theta power changes in the vmPFC preceded those observed in the hippocampus. These results constitute the first evidence in humans that episodic memory retrieval and scene imagination rely on similar vmPFC-hippocampus neural dynamics. Furthermore, they provide support for theories emphasising similarities between both cognitive processes, and perspectives that propose the vmPFC guides the construction of context-relevant representations in the hippocampus. Significance statementEpisodic memory retrieval is characterised by a dialogue between hippocampus and ventromedial prefrontal cortex (vmPFC). It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. An ensuing prediction would be of a comparable interaction between the two brain regions during the construction of novel scene imagery. Here, we leveraged the high temporal resolution of magnetoencephalography (MEG), and combined it with a scene imagination task. We found that a hippocampal-vmPFC dialogue existed, and that it took the form of vmPFC driving the hippocampus. We conclude that episodic memory and scene imagination share fundamental neural dynamics, and the process of constructing vivid, spatially coherent, contextually appropriate scene imagery is strongly modulated by vmPFC.

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Temporally discontinuous engagement of the vmPFC in remote memory retrieval

Systems-level consolidation refers to the time-dependent reorganisation of memory traces in the neocortex, a process in which the ventromedial prefrontal cortex (vmPFC) has been implicated. Capturing the precise temporal evolution of this crucial process in humans has long proved elusive. Here, we used multivariate methods and a longitudinal functional MRI design to detect, with high granularity, the extent to which autobiographical memories of different ages were represented in vmPFC and how this changed over time. We observed an unexpected time-course of vmPFC recruitment during retrieval, rising and falling around an initial peak of 8-12 months, before re-engaging for older two and five year old memories. This pattern was replicated in two independent sets of memories. Moreover, it was further replicated in a follow-up study eight months later with the same participants and memories, where the individual memory representations had undergone their hypothesised strengthening or weakening over time. We conclude that the temporal engagement of vmPFC in memory retrieval seems to be non-monotonic, revealing a complex relationship between systems-level consolidation and prefrontal cortex recruitment that is unaccounted for by current theories.\n\nAuthor SummaryOur past experiences are captured in autobiographical memories which allow us to recollect events from our lives long after they originally occurred. A part of the brains frontal lobe, called the ventromedial prefrontal cortex or vmPFC, is known to be important for supporting autobiographical memories especially as memories become more remote. The precise temporal profile of the vmPFCs involvement is unclear, yet this information is vital if we are to understand how memories change over time and the mechanisms involved. In this study we sought to establish the time-course of vmPFC engagement in the recollection of autobiographical memories while participants recalled memories of different ages during functional magnetic resonance imaging (fMRI). Using a method that detects brain activity patterns associated with individual memories, we found that memory-specific neural patterns in vmPFC became more distinct over the first few months after a memory was formed, but then this initial involvement of vmPFC subsided after one year. However, more remote memories (two years and older), appeared to re-engage vmPFC once again. This temporal profile is difficult to accommodate within any single existing theory. Consequently, our results provoke a re-think about how memories evolve over time and the role played by the vmPFC.

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