Biology subjects

Hanslmayr, S.

Publications and source records attributed to Hanslmayr, S..

43 records · Page 3Linked to original sources

bioRxiv2018

Hippocampal synchrony and neocortical desynchrony cooperate to encode and retrieve episodic memories

Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these two processes are thought to be supported by neocortical alpha/beta desynchronisation and hippocampal theta/gamma synchronisation, respectively. Intuitively, these two processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analysing human intracranial EEG data recorded during two associative memory tasks. We find that neocortical alpha/beta (8-20Hz) power decreases reliably precede and predict hippocampal \"fast\" gamma (60-80Hz) power increases during episodic memory formation; during episodic memory retrieval however, hippocampal \"slow\" gamma (40-50Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from neocortex to hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.\n\nSignificance StatementEpisodic memories detail our personally-experienced past. The formation and retrieval of these memories has long been thought to be supported by a division of labour between the neocortex and the hippocampus, where the former processes event-related information and the latter binds this information together. However, it remains unclear how the two regions interact. We uncover directional coupling between these regions, with power decreases in the neocortex that precede and predict power increases in the hippocampus during memory formation. Fascinatingly, this process reverses during memory retrieval, with hippocampal power increases preceding and predicting neocortical power decreases. These results suggest a bidirectional flow of information between the neocortex and hippocampus is fundamental to the formation and retrieval of episodic memories.

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bioRxiv2018

Single-trial Phase Entrainment of Theta Oscillations in Sensory Regions Predicts Human Associative Memory Performance

Episodic memories are rich in sensory information and often contain integrated information from different sensory modalities. For instance, we can store memories of a recent concert with visual and auditory impressions being integrated in one episode. Theta oscillations have recently been implicated in playing a causal role synchronizing and effectively binding the different modalities together in memory. However, an open question is whether momentary fluctuations in theta synchronization predict the likelihood of associative memory formation for multisensory events. To address this question we presented movies and sounds with their luminance and volume modulated at theta (4 Hz), with a phase offset at 0{degrees} or 180{degrees} with respect to each other. This allowed us to entrain the visual and auditory cortex in a synchronous (0{degrees}) or asynchronous manner (180{degrees}). Participants were asked to remember the association between a movie and a sound while having their EEG activity recorded. Associative memory performance was significantly enhanced in the synchronous (0{degrees}) compared to the asynchronous (180{degrees}) condition. Source-level analysis demonstrated that the physical stimuli effectively entrained their respective cortical areas with a corresponding phase offset. Importantly, the strength of entrainment during encoding correlated with the efficacy of associative memory such that small phase differences between visual and auditory cortex predicted a high likelihood of correct retrieval in a later recall test. These findings suggest that theta oscillations serve a specific function in the episodic memory system: Binding the contents of different modalities into coherent memory episodes.\n\nSignificance StatementHow multi-sensory experiences are bound to form a coherent episodic memory representation is one of the fundamental questions in human episodic memory research. Evidence from animal literature suggests that the relative timing between an input and theta oscillations in the hippocampus is crucial for memory formation. We precisely controlled the timing between visual and auditory stimuli and the neural oscillations at 4 Hz using a multisensory entrainment paradigm. Human associative memory formation depends on coincident timing between sensory streams processed by the corresponding brain regions. We provide evidence for a significant role of relative timing of neural theta activity in human episodic memory on a single trial level, which reveals a crucial mechanism underlying human episodic memory.

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bioRxiv2018

Reactivation of neural patterns during memory reinstatement supports encoding specificity

Encoding specificity or transfer appropriate processing state that memory benefits when items are encoded and retrieved in the same modality compared to when encoding and retrieval is conducted in different modalities. In neural terms, these effects can be expressed by a resonance process between a memory cue and a stored engram; the more the two overlap the better memory performance. We here used temporal pattern analysis in MEG to tap into this resonance process. We predicted that reactivation of sensory patterns established during encoding has opposing effects depending on whether there is a match or mismatch between the memory cue and the encoding modality. To test this prediction items were presented either visually or aurally during encoding and in a recognition test to create match (e.g. \"dog\" presented aurally during encoding and recognition) and mismatch conditions (e.g. \"dog\" presented aurally during encoding and shown visually during recognition). Memory performance was better for items in the match compared to the mismatch condition. MEG results showed that memory benefitted from neural pattern reinstatement only in the match condition, but suffered from reinstatement in the mismatch condition. These behavioural and neural effects were asymmetric in that they were only obtained for aurally encoded words but not for visually encoded words. A simple computational model was generated in order to simulate these opposing effects of neural pattern reactivation on memory performance. We argue that these results suggest that reactivation of neural patterns established during encoding underlies encoding specificity or transfer appropriate processing.

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bioRxiv2017

Replay of Stimulus Specific Temporal Patterns during Associative Memory Formation

Forming a memory often entails the association of recent experience with present events. This recent experience is usually an information rich and dynamic representation of the world around us. We here show that associating a static cue with a previously shown dynamic stimulus, yields a detectable, dynamic representation of this stimulus in working memory. We further implicate this representation in the decrease of low-frequency power ([~]4-30 Hz) in the ongoing electroencephalogram (EEG), which is a well-known correlate of successful memory formation. The maintenance of content specific patterns in desynchronizing brain oscillations was observed in two sensory domains, i.e. in a visual and in an auditory condition. Together with previous results, these data suggest a mechanism that generalizes across domains and processes, in which the decrease in oscillatory power allows for the dynamic representation of information in ongoing brain oscillations.

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bioRxiv2017

Across-subjects classification of stimulus modality from human MEG high frequency activity

Single-trial analyses have the potential to uncover meaningful brain dynamics that are obscured when averaging across trials. However, low signal-to-noise ratio (SNR) can impede the use of single-trial analyses and decoding methods. In this study, we investigate the applicability of a single-trial approach to decode stimulus modality from magnetoencephalography (MEG) high frequency activity. In order to classify the auditory versus visual presentation of words, we combine beamformer source reconstruction with the random forest classification method. To enable group level inference, the classification is embedded in an across-subjects framework.\n\nWe show that single-trial gamma SNR allows for good classification performance (accuracy across subjects: 66.44 %). This implies that the characteristics of high frequency activity have a high consistency across trials and subjects. The random forest classifier assigned informational value to activity in both auditory and visual cortex with high spatial specificity. Across time, gamma power was most informative during stimulus presentation. Among all frequency bands, the 75-95 Hz band was the most informative frequency band in visual as well as in auditory areas. Especially in visual areas, a broad range of gamma frequencies (55-125 Hz) contributed to the successful classification.\n\nThus, we demonstrate the feasibility of single-trial approaches for decoding the stimulus modality across subjects from high frequency activity and describe the discriminative gamma activity in time, frequency, and space.\n\nAuthor SummaryAveraging brain activity across trials is a powerful way to increase signal-to-noise ratio in MEG data. This approach, however, potentially obscures meaningful brain dynamics that unfold on the single-trial level. Single-trial analyses have been successfully applied to time domain or low frequency oscillatory activity; its application to MEG high frequency activity is hindered by the low amplitude of these signals. In the present study, we show that stimulus modality (visual versus auditory presentation of words) can successfully be decoded from single-trial MEG high frequency activity by combining source reconstruction with a random forest classification algorithm. This approach reveals patterns of activity above 75 Hz in both visual and auditory cortex, highlighting the importance of high frequency activity for the processing of domain-specific stimuli. Thereby, our results extend prior findings by revealing high-frequency activity in auditory cortex related to auditory word stimuli in MEG data. The adopted across-subjects framework furthermore suggests a high inter-individual consistency in the high frequency activity patterns.

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bioRxiv2017

The Sync/deSync model: How a synchronized hippocampus and a de-synchronized neocortex code memories

Neural oscillations are important for memory formation in the brain. The de-synchronisation of Alpha (10Hz) oscillations in the neo-cortex has been shown to predict successful memory encoding and retrieval. However, when engaging in learning, it has been found that the hippocampus synchronises in Theta (4Hz) oscillations, and that learning is dependent on the phase of Theta. This inconsistency as to whether synchronisation is good for memory formation leads to confusion over which oscillations we should expect to see and where during learning paradigm experiments. This paper seeks to respond to this inconsistency by presenting a neural network model of how a well-functioning learning system could exhibit both of these phenomena, i.e. desynchronization of alpha and synchronisation of theta during successful memory encoding.\n\nWe present a spiking neural network (the Sync/deSync model) of the neo-cortical and hippocampal system. The simulated hippocampus learns through an adapted spike-time dependent plasticity rule, in which weight change is modulated by the phase of an extrinsically generated theta oscillation. Additionally, a global passive weight decay is incorporated, which is also modulated by theta phase. In this way, the Sync/deSync model exhibits theta phase-dependent long-term potentiation and long-term depression. We simulated a learning paradigm experiment and compared the oscillatory dynamics of our model with those observed in single-cell and scalp-EEG studies of the medial temporal lobe. Our Sync/deSync model suggests that both the de-synchronisation of neo-cortical Alpha and the synchronisation of hippocampal Theta are necessary for successful memory encoding and retrieval.\n\nSignificance statementA fundamental question is the role of rhythmic activation of neurons, i.e. how their firing oscillates between high and low rates. A particularly important question is how oscillatory dynamics between the neo-cortex and hippocampus contribute to memory formation. We present a spiking neural-network model of such memory formation, with the central ideas that 1) in neo-cortex, neurons need to break-out of an alpha oscillation in order to represent a stimulus (i.e. alpha desynchronises), while 2) in hippocampus, the firing of neurons at theta facilitates formation of memories (i.e. theta synchronises). Accordingly, successful memory formation is marked by reduced neo-cortical alpha and increased hippocampal theta. This pattern has been observed experimentally and gives our model its name - the Synch/deSynch model.

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bioRxiv2017

Data-driven re-referencing of intracranial EEG based on independent component analysis (ICA)

Intracranial recordings from patients implanted with depth electrodes are a valuable source of information in cognitive neuroscience. They allow for the unique opportunity to record brain activity with a high spatial and temporal resolution. To extract the local signal of interest in stereotactic EEG (S-EEG) data, a common pre-processing choice is to re-reference the data with a bipolar montage.\n\nWith bipolar reference, each channel is subtracted from its neighbour in order to reduce commonalities between channels and isolate activity that is spatially confined. We here challenge the assumption that bipolar reference can effectively perform this task. We argue that in order to extract local activity, the distribution of the signal source of interest, as well as the distribution of interfering distant signals and noise sources need to be considered. Those can have a variable spatial extent and are modulated by electrode spacing, location and anatomical characteristics. Those factors are not accounted for by a fixed referencing scheme and bipolar reference can therefore not only decrease the signal to noise ratio (SNR) of the data, but also lead to mislocalization of activity and consequently to misinterpretation of results.\n\nWe promote the perspective of regarding referencing as a spatial filtering operation with fixed coefficients. As an alternative, we propose to use Independent Component Analysis (ICA), to derive filter coefficients that reflect the statistical dependencies of the data at hand. We argue that ICA performs the same task that bipolar referencing pursues, namely undoing the linear superposition of activity and can therefore be used to identify activity that is local. We first describe and demonstrate this procedure on human S-EEG recordings. In a simulation with real data, we then quantitatively show that ICA outperforms the bipolar referencing operation in sensitivity and importantly in specificity when it comes to revealing local time series from the superposition of neighbouring channels.

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