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Reber, T. P.

Publications and source records attributed to Reber, T. P..

10 recordsLinked to original sources

Input-space geometry shapes adaptation dynamics underlying repetition suppression in a neural network model of relatedness priming

A key function of the human brain is its ability to dynamically adapt to novel contexts by integrating prior experience. While neural adaptation is widely observed across cortical systems, the microcircuit-level mechanisms governing its intensity and temporal dynamics remain unclear. To bridge this gap, we develop a recurrent network of adaptive exponential integrate-and-fire neurons governed by a triplet spike-timing-dependent plasticity rule, designed to reproduce neural dynamics recorded via intracranial electrophysiology and single-unit recordings from the medial temporal lobe of neurosurgical patients performing a priming task. Using input organizations inspired by the experimental paradigm, we systematically vary input geometry to investigate its impact on adaptation dynamics. We find that neural adaptation emerges from recurrent dynamics shaped by learned connectivity, with both its magnitude and temporal profile depending on the geometry of the input space. This dependence gives rise, at the simulated single-neuron level, to a continuum of response regimes ranging from sharpening-like to fatiguing-like dynamics. Sharpening-like responses dominate when inputs exhibit high within-meta-category similarity and strong between-meta-category separation, whereas fatiguing-like responses emerge under the opposite regime.

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Sleep ripples drive single-neuron reactivation for human memory consolidation

Sleep transforms fragile experiences into lasting memories, but the neuronal basis of this process in humans has remained elusive. In rodents, hippocampal ripples orchestrate the replay of place cell sequences, establishing a cellular mechanism for consolidation - though with limited generalizability to human memory. In humans, neuroimaging has revealed large-scale offline reactivation, but these coarse signals leave open whether individual neurons are reactivated and how ripples might mediate this process. Here, we bridge this gap by directly recording 1,466 medial temporal lobe (MTL) neurons and intracranial electroencephalography during learning, post-learning wakefulness, and sleep. We show that ripples robustly drive neuronal firing, with sleep ripples eliciting stronger activation than wake ripples. Critically, neurons tuned to items that were later remembered fired more strongly during ripples than those coding for forgotten items, and this memory-linked reactivation was selectively observed during sleep. Finally, ripple-associated neuronal MTL bursts were detectable across widespread cortical activity, pointing to a mechanism for systems-level consolidation. Together, these findings provide the first direct evidence that ripple-driven single-neuron reactivation supports human episodic memory consolidation and reveal why sleep -- compared to wakefulness -- offers a privileged window for stabilizing memories.

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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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Proficiency-Dependent and Dynamic Reorganization of Brain Networks During Children's Second Language Learning

Childrens second language (L2) vocabulary learning is often indexed with event-related potentials (ERPs) by the N400 incongruity effect, yet its stability in real classrooms is unclear. We recorded 64-channel EEG from 42 children (aged 9-15 years) during a translation-recognition task before and after a regular instructional vocabulary unit and sub-grouped children by baseline proficiency. We quantified the canonical N400 (300-500 ms, centroparietal region of interest; ROI) alongside electrical-neuroimaging indices of ERP strength and topography (Global Field Power, Global Map Dissimilarity, ERP template-map preponderance), using adult template maps from a prior study as a normative reference. Behaviorally, children showed large gains in vocabulary accuracy and higher discrimination sensitivity (d') in post-assessment. The classical N400 incongruity effect did not increase from pre- to post-learning. By contrast, global and topographic measures were learning-sensitive: Global Field Power increased across sessions and interacted with proficiency, and Global Map Dissimilarity showed main effects of session and proficiency as well as their interaction, indicating proficiency-dependent topographic reorganization. Adult normative template maps backfitted well; within the N400 window, high-proficiency children more consistently occupied an adult-like configuration; later ([~]650-800 ms), patterns also differentiated by proficiency and congruency. Relative to adults, children exhibited more diffuse topographies and stronger dependence on individual proficiency. In classroom settings, childrens L2 vocabulary learning is therefore more sensitively indexed by scalp topography and global field dynamics than by a single N400 amplitude, positioning electrical neuroimaging as a proficiency-dependent, classroom-relevant marker of L2 acquisition.

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Semantic Tuning of Single Neurons in the Human Medial Temporal Lobe

The Medial Temporal Lobe (MTL) is key to human cognition, supporting memory, emotional processing, navigation, and semantic coding. Rare direct human MTL recordings revealed concept cells, which were proposed as episodic memory building blocks due to their context- and modality-invariant response. However, there is a long-standing debate whether concept cells encode information in a discrete, all-or-none fashion, or as a graded, continuous function of semantic dimensions. To resolve this, we developed a closed-loop protocol that analyzes neuronal spiking in real time and adaptively presents new stimuli based on semantic similarity to response-eliciting previous ones. We found that human concept cells show graded responses, following semantic tuning curves. Furthermore, the tuning width and steepness of MTL neurons vary, with the hippocampus exhibiting the steepest tuning. Regional analysis of these tuning curves yields region-specific categorical response profiles (e.g., food responses in the amygdala). Finally, we show that at the population level, MTL activity is best captured by continuous semantic vector models, which outperform categorical and network-based metrics. Together, these findings establish that concept cells exhibit semantic tuning curves, providing new mechanistic insights into the neural organization of semantic information in the human brain.

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Brain Network Differences in Second Language Learning Depend on Individual Competencies

Integrating new words into an existing semantic network is a core challenge of second language (L2) acquisition. We investigated how evidence-based learning strategies and individual performance shape the neurocognitive dynamics of vocabulary learning. Eighty- three adults with German or French as their native language (L1) learned 48 Finnish (L2) nouns over 14 days using a mobile app that systematically varied retrieval practice, corrective feedback, multisensory learning, and distributed learning. Before and after training, EEG was recorded during a translation recognition task designed to elicit the N400, an index of semantic integration. Vocabulary accuracy increased from 0.41% pre-learning to 75.5% post- learning (dz = 3.96), and the N400 incongruity effect increased significantly, F(1, 75) = 99.52, p < .001, {superscript 2}g = .32, reflecting successful integration of new L2 words into the mental lexicon. High performers showed larger N400 responses and distinct ERP template-map preponderance (i.e., the proportion of epoch time points assigned to a given template map) indicating more efficient and specialized neural processing. Despite systematic manipulation of learning strategies, no single approach yielded consistent behavioral or neural advantages, suggesting that overall exposure and cumulative practice--rather than any specific strategy-- were the key drivers of robust learning. ERP template-map analyses further revealed that learning not only amplified neural responses but also shifted the preponderance of maps in the N400 window, signaling a qualitative reorganization of semantic processing. These findings bridge cognitive neuroscience and language education, suggesting that the depth and success of vocabulary learning may depend more on the degree of integration achieved than on the specific instructional strategy employed.

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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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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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A key role of the hippocampal P3 in the attentional blink

The attentional blink (AB) refers to an impaired identification of target stimuli (T2), which are presented shortly after a prior target (T1) within a rapid serial visual presentation (RSVP) stream. It has been suggested that the AB is related to a failed transfer of T2 into working memory and that hippocampus (HC) and entorhinal (EC) cortex are regions crucial for this transfer. Since the event-related P3 component has been linked to inhibitory processes, we hypothesized that the hippocampal P3 elicited by T1 may impact on T2 processing within HC and EC. To test this hypothesis, we reanalyzed microwire data from 21 patients, who performed an RSVP task, during intracranial recordings for epilepsy surgery assessment (Reber et al., 2017). We identified T1-related hippocampal P3 components in the local field potentials (LFPs) and determined the temporal onset of T2 processing in HC/EC based on single-unit response onset activity. In accordance with our hypothesis, T1-related single-trial P3 amplitudes at the onset of T2 processing were clearly larger for unseen compared to seen T2-stimuli. Moreover, increased T1-related single-trial P3 peak latencies were found for T2[unseen] versus T2[seen] trials in case of lags 1 to 3, which was in line with our predictions. In conclusion, our findings support inhibition models of the AB and indicate that the hippocampal P3 elicited by T1 plays a central role in the AB.

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Auditory beat stimulation modulates memory-related single-neuron activity in the human medial temporal lobe

Auditory beats are composed of two sine waves using nearby frequencies, which can either be applied as a superposed signal to both ears or to each ear separately. In the first case, the beat sensation results from hearing an amplitude-modulated signal (monaural beat). In the second case, it is generated by phase-sensitive neurons in the brain stem (binaural beat). We investigated the effects of monaural and binaural 5 Hz beat stimulation on neural activity and memory performance in neurosurgical patients performing an associative recognition task. Previously, we had reported that these beat stimulation conditions modulated memory performance in opposite directions. Here, we analyzed data from a patient subgroup, in which microwires were implanted in the amygdala, hippocampus, entorhinal cortex and parahippocampal cortex. We identified neurons responding with firing rate changes to binaural versus monaural 5 Hz beat stimulation. In these neurons, we correlated the differences in firing rates for binaural versus monaural beats to the memory-related differences for remembered versus forgotten items and associations. In the left hemisphere for these neurons, we detected statistically significant negative correlations between firing rate differences for binaural versus monaural beats and remembered versus forgotten items/associations. Importantly, such negative correlations were also observed between beat stimulation-related firing rate differences in the baseline window and memory-related firing rate differences in the poststimulus windows. In line with concepts of homeostatic plasticity, we interpret our findings as indicating that beat stimulation is linked to memory performance via shifting baseline firing levels.

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