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Niediek, J.

Publications and source records attributed to Niediek, J..

9 recordsLinked to original sources

Sequential coupling of sleep oscillations enables concept-neuron reactivation and supports information flow across the human hippocampal-cortical circuit

Effective memory consolidation during sleep is thought to rely on the transfer of reactivated memory traces from the hippocampus to the cortex. However, the mechanisms supporting this essential dialogue across brain areas remain poorly understood. Here, we recorded single-neuron activity (n = 1097) in the medial temporal lobe (MTL) of 10 epilepsy patients across 21 nights of sleep. Before sleep, patients engaged in a memory task with stimuli eliciting concept-neuron responses. During non-rapid eye movement (NREM) sleep, neuronal firing locked to sharp wave-ripples (SWR) revealed a directed flow of information from the hippocampus to cortical targets. Notably, within SWR-driven activity, experience-dependent concept neurons exhibited elevated co-activation both within and across MTL regions, indicating selective reactivation of behaviorally relevant information. Cross-regional co-activation of concept cells was markedly enhanced when hippocampal SWRs coincided with cortical slow oscillation-spindle complexes, suggesting an active role of the cortex in shaping interregional communication. These findings provide evidence that SWRs in humans selectively reactivate experience-related neural ensembles across the hippocampal-cortical network, while synergistic interactions with cortical slow oscillation-spindle events might facilitate effective memory consolidation.

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Episodic memory consolidation by reactivation of human concept neurons during sleep reflects contents, not sequence of events

How do our brains manage to store our everyday experiences into memory? Neurons in the human temporal lobe that respond to the concept of an individual person or object have been shown to provide the semantic building blocks for episodic memory. Recording from 1433 neurons in neurosurgical patients who learned a story involving specific concepts, we found reactivation of neurons representing these concepts during slow-wave sleep after learning. Concept neurons were conjointly reactivated, particularly during sharp-wave ripples, with time lags suitable for synaptic modification. However, the temporal sequence of reactivation did not reflect the sequence of concepts in the learned story. Unlike rodent place cells, which can acquire preferred firing locations during exploration of new environments according to their pre-existing preferred sequence of activation, human concept neurons are tuned to specific semantic contents before learning starts. Consequently, pre-existing firing sequences correlate with consecutive place fields in rodents, but not with sequences of events in human experience. Thus, in contrast to reactivation of rodent place cells, reactivation of human concept cells does not reflect sequences of events in human experience.

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Gamma - Theta - Spike Coupling Coordinates Sequential Memory in Human MTL

It has been suggested that hierarchical synchronization of theta and gamma oscillations coordinates neural activity during sequence memory. Yet, the role of gamma oscillations and their interaction with theta and single-unit activity (SUA) has not been directly examined in humans. We analysed simultaneous micro wire recordings of single-unit activity (N = 1417) and local field potentials (N = 917 channels) from the medial temporal lobe (MTL) of epilepsy patients performing a visual multi-item sequence memory task. During encoding, both spiking activity and gamma power contained item-specific information and were temporally coupled. During memory maintenance, stimulus-specific gamma was characterized by recurring bursts during which spiking was tightly synchronized and both, gamma and spiking, were preferentially aligned to similar theta phases predictive of sequential stimulus position. These findings demonstrate that theta-gamma-spike interactions support a phase-based multiplexed code for sequential memories in the human MTL.

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Insular cortex encodes task alignment

Animals can learn complex behaviors. Animal behavior in the lab has traditionally been studied via summary statistics such as trial-based success rates. However, animal behavior is much more fine-grained: a trial in an experiment often consists of multiple actions, and more than one strategy can lead to a successful completion of a trial. To understand how the brain controls behavior, a fine-grained yet compact description of behavior is necessary. We describe here an approach for estimating the strategies animals use for a large family of tasks from first principles. Using reinforcement learning with informational constraints on policies, we compute a rich set of candidate policies with a small number of meaningful parameters, and match observed behavior to these policies. In a sample rat task, our approach revealed ongoing learning for more than 100 days after the saturation of success rates. Moreover, we showed that many neurons in the insular cortex of rats track the instantaneous task engagement of the rats with a resolution of a few minutes. Due to its generic formulation in reinforcement learning terminology, our work is directly applicable to the majority of animal tasks in use today.

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Task-related activity in auditory cortex enhances sound representation

In auditory-guided tasks, sound presentations often occupy a small fraction of the total task time. We studied here neuronal dynamics that spanned trial duration. Many neurons had large, slow, firing rate modulations, which were not driven by sounds, were larger than the sound evoked responses, and were locked to specific time points during the task, similar to responses of hippocampal time-sensitive neurons. Concurrently, responses to sounds differed between active behavior and passive listening conditions: in the active sessions, the on-going activity just before sound presentations was higher and the responses to target stimuli were weaker but more informative about the task-relevant sounds. We show that the slow firing rate modulations caused the increased on-going activity. Using a model, we demonstrate that higher on-going activity led to more synaptic depression of the cortico-cortical synapses, reducing the tendency to produce population spikes and resulting in weaker but more informative responses.

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Decoding movie content from neuronal population activity in the human medial temporal lobe

The human medial temporal lobe (MTL), a region implicated in memory and high-level cognition, contains neurons that respond selectively to stimuli belonging to specific categories, such as individual people, landmarks, or objects. However, these neurons have been largely studied via static, isolated presentations of stimuli. Therefore, it is unclear how neurons in the MTL respond to rich stimuli such as movies, and which dynamical stimulus features can be retrieved from neuronal population spiking activity. We studied single-unit responses from 2286 neurons recorded from the amygdala, hippocampus, entorhinal cortex, and parahippocampal cortex of 29 intracranially implanted patients during the presentation of an 83-minute movie. We found only a few individual neurons that exhibited a classic selective response to semantic features. However, we successfully decoded the presence of characters, settings, and visual transitions from neuronal population activity. The information relevant for decoding varies across regions depending on the feature category, as visual transitions could be decoded from subsets of neurons with selective responses, whereas character and location features relied on distributed representations. Our results demonstrate an approach for reliably decoding movie features in the human MTL, and suggest that the brain uses a population code when representing character and location features.

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How coupled slow oscillations, spindles and ripples control neuronal processing and communication during human sleep

Learning and plasticity rely on fine-tuned regulation of neuronal circuits during offline periods. An unresolved puzzle is how the sleeping brain - in the absence of external stimulation or conscious effort - controls neuronal firing rates (FRs) and communication within and across circuits, supporting synaptic and systems consolidation. Using intracranial Electroencephalography (iEEG) combined with multiunit activity (MUA) recordings from the human hippocampus and surrounding medial temporal lobe (MTL) areas, we here show that governed by slow oscillation (SO) up-states, sleep spindles set a timeframe for ripples to occur. This sequential coupling leads to a stepwise increase in (i) neuronal FRs, (ii) short-latency cross-correlations among local neuronal assemblies and (iii) cross-regional MTL interactions. Triggered by SOs and spindles, ripples thus establish optimal conditions for spike-timing dependent plasticity and systems consolidation. These results unveil how the coordinated coupling of specific sleep rhythms orchestrates neuronal processing and communication during human sleep.

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Phase of firing does not reflect temporal order in sequence memory of humans and recurrent neural networks

A prominent theory proposes that the temporal order of a sequence of items held in memory is reflected in ordered firing of neurons at different phases of theta oscillations 1. We probe this theory by directly measuring single neuron activity (1420 neurons) and local field potentials (LFP, 921 channels) in the medial temporal lobe of 16 epilepsy patients performing a working memory task for temporal order. We observe theta oscillations and preferential firing of single neurons at theta phase during memory maintenance. We find that - depending on memory performance - phase of firing is related to item position within a sequence. However, in contrast to the theory, phase order did not match item order. To investigate underlying mechanisms, we subsequently trained recurrent neural networks (RNNs) to perform an analogous task. Similar to recorded neural activity, we show that RNNs generate theta oscillations during memory maintenance. Importantly, model neurons exhibit theta phase-dependent firing related to item position, where phase of firing again did not match item order. Instead, we observed a mechanistic link between phase order, stimulus timing and oscillation frequency - a relationship we subsequently confirmed in our neural recordings. Taken together, in both biological and artificial neural networks we provide validating evidence for the role of phase-of-firing in memory processing while at the same time challenging a long-held theory about the functional role of spiking and oscillations in sequence memory.

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The RIFF: an automated environment for studying the neural basis of auditory-guided complex behavior

Behavior consists of the interaction between an organism and its environment, and is controlled by the brain. Brain activity varies at sub-second time scales, but behavioral measures are usually coarse (often consisting of only binary trial outcomes). To overcome this mismatch, we developed the RIFF: a programmable interactive arena for freely-moving rats with multiple feeding areas, multiple sound sources, high-resolution behavioral tracking, and simultaneous electrophysiological recordings. We describe two complex tasks implemented in the RIFF. Rats quickly learned these tasks and developed anticipatory behavior. Neurons in auditory cortex and posterior insula showed sensitivity to non-auditory parameters such as location and pose. Our combination of wireless electrophysiology and detailed behavioral documentation in a controlled environment produces insights into the cognitive capabilities and learning mechanisms of rats and opens the way to a better understanding of how brains control behavior.

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