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Knight, R. T.

Publications and source records attributed to Knight, R. T..

At least 55 records · Page 3Linked to original sources

Multiple memory systems for efficient temporal order memory

We report the distinct contribution of multiple memory systems to retrieval of the temporal order of events. The neural dynamics related to retrieval of movie scenes revealed that recalling the temporal order of close events elevates hippocampal theta power, like that observed for recalling close spatial relationships. In contrast, recalling far events elevates beta power in the orbitofrontal cortex, reflecting recall based on the overall movie structure.

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Human REM sleep controls neural excitability in support of memory formation

Sleep oscillations provide a key substrate to facilitate memory processing, the underlying mechanism of which may involve the overnight homeostatic regulation of plasticity at a synaptic and whole-network level. However, there remains a lack of human data demonstrating if and how sleep enhances memory consolidation and associated neural homeostasis. We combined intracranial recordings and scalp electroencephalography (EEG) in humans to reveal a new role for rapid eye movement (REM) sleep in promoting the homeostatic recalibration of optimal excitation/inhibition-balance. Moreover, the extent of this REM-sleep homeostatic recalibration predicted the success of overnight memory consolidation, expressly the modulation of hippocampal-- neocortical excitability favoring remembering rather than forgetting. The findings describe a novel, fundamental role of human REM sleep in maintaining neural homeostasis, thereby enhancing long-term memory.

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Encoding and decoding analysis of music perception using intracranial EEG

Music perception engages multiple brain regions, however the neural dynamics of this core human experience remains elusive. We applied predictive models to intracranial EEG data from 29 patients listening to a Pink Floyd song. We investigated the relationship between the song spectrogram and the elicited high-frequency activity (70-150Hz), a marker of local neural activity. Encoding models characterized the spectrotemporal receptive fields (STRFs) of each electrode and decoding models estimated the population-level song representation. Both methods confirmed a crucial role of the right superior temporal gyri (STG) in music perception. A component analysis on STRF coefficients highlighted overlapping neural populations tuned to specific musical elements (vocals, lead guitar, rhythm). An ablation analysis on decoding models revealed the presence of unique musical information concentrated in the right STG and more spatially distributed in the left hemisphere. Lastly, we provided the first song reconstruction decoded from human neural activity.

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Population coding and oscillatory subspace synchronization integrate context into actions

Contextual cues and prior evidence guide human goal-directed behavior. To date, the neurophysiological mechanisms that implement contextual priors to guide subsequent actions remain unclear. Here we demonstrate that increasing behavioral uncertainty introduces a shift from an oscillatory to a continuous processing mode in human prefrontal cortex. At the population level, we found that oscillatory and continuous dynamics reflect dissociable signatures that support distinct aspects of encoding, transmission and execution of context-dependent action plans. We show that prefrontal population activity encodes predictive context and action plans in serially unfolding orthogonal subspaces, while prefrontal-motor theta oscillations synchronize action-encoding population subspaces to mediate the hand-off of action plans. Collectively, our results reveal how two key features of large-scale population activity, namely continuous population trajectories and oscillatory synchrony, operate in concert to guide context-dependent human behavior.

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Awake ripples enhance emotional memory encoding in the human brain

Intracranial recordings from the human amygdala and the hippocampus during an emotional memory encoding and discrimination task reveal increased awake sharp-wave/ripples (aSWR) after encoding of emotional compared to neutral stimuli. Further, post-encoding aSWR-locked memory reinstatement in the amygdala and the hippocampus was predictive of later memory discrimination. These findings provide electrophysiological evidence that post-encoding aSWRs enhance memory for emotional events.

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Direct brain recordings reveal continuous encoding of structure in random stimuli

The brain excels at processing sensory input, even in rich or chaotic environments. Mounting evidence attributes this to the creation of sophisticated internal models of the environment that draw on statistical structures in the unfolding sensory input. Understanding how and where this modeling takes place is a core question in statistical learning and predictive processing. In this context, we address the role of transitional probabilities as an implicit structure supporting the encoding of a random auditory stream. Leveraging information-theoretical principles and the high spatiotemporal resolution of intracranial electroencephalography, we analyzed the trial-by-trial high-frequency activity representation of transitional probabilities. This unique approach enabled us to demonstrate how the brain continuously encodes structure in random stimuli and revealed the involvement of a network outside of the auditory system, including hippocampal, frontal, and temporal regions. Linking the frame-works of statistical learning and predictive processing, our work illuminates an implicit process that can be crucial for the swift detection of patterns and unexpected events in the environment.

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Consciousness is supported by near-critical cortical electrodynamics

Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition, and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, for the first time, we empirically identify the specific critical point near which conscious cortical dynamics operate as the edge-of-chaos critical point, or the boundary between periodicity/stability and chaos/instability. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magne-toencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, GABAergic anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of cortical dynamics away from this critical point; conversely, we show that psychedelics may increase the information-richness of cortical activity by tuning cortical electrodynamics closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC), and show that assessing the proximity of cortical electrodynamics to the edge-of-chaos critical point may be clinically useful as a new biomarker of consciousness. Significance StatementWhat changes in the brain when we lose consciousness? One possibility is that the loss of consciousness corresponds to a transition of the brains electric activity away from edge-of-chaos criticality, or the knifes edge in between stability and chaos. Recent mathematical developments have produced novel tools for testing this hypothesis, which we apply for the first time to cortical recordings from diverse brain states. We show that the electric activity of the cortex is indeed poised near the boundary between stability and chaos during conscious states and transitions away from this boundary during unconsciousness, and that this transition disrupts cortical information processing.

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Left Hemisphere Dominance for Bilateral Kinematic Encoding in the Human Brain

Neurophysiological studies in humans and non-human primates have revealed movement representations in both the contralateral and ipsilateral hemisphere. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography (ECoG) was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

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Modeling intracranial electrodes

BackgroundIntracranial electrodes are implanted in patients with drug-resistant epilepsy as part of their pre-surgical evaluation. This allows investigation of normal and pathological brain functions with excellent spatial and temporal resolution. The spatial resolution relies on methods that precisely localize the implanted electrodes in the cerebral cortex, which is critical for drawing valid anatomical inferences about brain function. Multiple methods have been developed to localize implanted electrodes, mainly relying on pre-implantation MRI and post-implantation CT images. However, there is no standard approach to quantify the performance of these methods systematically. The purpose of our work is to model intracranial electrodes to simulate realistic implantation scenarios, thereby providing methods to optimize localization algorithm performance. ResultsWe implemented novel methods to model the coordinates of implanted grids, strips, and depth electrodes, as well as the CT artifacts produced by these. We successfully modeled a large number of realistic implantation "scenarios", including different sizes, inter-electrode distances, and brain areas. In total, more than 3300 grids and strips were fitted over the brain surface, and more than 850 depth electrode arrays penetrating the cortical tissue were modeled. More than 37000 simulations of electrode array CT artifacts were performed in these "scenarios", mimicking the intensity profile and orientation of real artifactual voxels. Realistic artifacts were simulated by introducing different noise levels, as well as overlapping electrodes. ConclusionsWe successfully developed the first platform to model implanted intracranial grids, strips, and depth electrodes and realistically simulate CT artifacts and noise. These methods set the basis for developing more complex models, while simulations allow the performance evaluation of electrode localization techniques systematically. The methods described in this article, and the results obtained from the simulations, are freely available via open repositories. A graphical user interface implementation is also accessible via the open-source iElectrodes toolbox.

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Dissociable oscillatory networks support gain and loss processing in human orbitofrontal cortex

Human neuroimaging and animal studies have linked neural activity in orbitofrontal cortex (OFC) to valuation of positive and negative outcomes. Additional evidence shows that neural oscillations, representing the coordinated activity of neuronal ensembles, support information processing in both animal and human prefrontal regions. However, the role of OFC neural oscillations in reward-processing in humans remains unknown, partly due to the difficulty of recording oscillatory neural activity from deep brain regions. Here, we examined the role of OFC neural oscillations (<30Hz) in reward processing by combining intracranial OFC recordings with a gambling task in which patients made economic decisions under uncertainty. Our results show that power in different oscillatory bands are associated with distinct components of reward evaluation. Specifically, we observed a double dissociation, with a selective theta band oscillation increase in response to monetary gains and a beta band increase in response to losses. These effects were interleaved across OFC in overlapping networks and were accompanied by increases in oscillatory coherence between OFC electrode sites in theta and beta band during gain and loss processing, respectively. These results provide evidence that gain and loss processing in human OFC are supported by distinct low-frequency oscillations in networks, and provide evidence that participating neuronal ensembles are organized functionally through oscillatory coherence, rather than local anatomical segregation.

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Imagined speech can be decoded from low- and cross-frequency features in perceptual space

Reconstructing intended speech from neural activity using brain-computer interfaces (BCIs) holds great promises for people with severe speech production deficits. While decoding overt speech has progressed, decoding imagined speech have met limited success, mainly because the associated neural signals are weak and variable hence difficult to decode by learning algorithms. Using three electrocorticography datasets totalizing 1444 electrodes from 13 patients who performed overt and imagined speech production tasks, and based on recent theories of speech neural processing, we extracted consistent and specific neural features usable for future BCIs, and assessed their performance to discriminate speech items in articulatory, phonetic, vocalic, and semantic representation spaces. While high-frequency activity provided the best signal for overt speech, both low- and higher-frequency power and local cross-frequency contributed to successful imagined speech decoding, in particular in phonetic and vocalic, i.e. perceptual, spaces. These findings demonstrate that low-frequency power and cross-frequency dynamics contain key information for imagined speech decoding, and that exploring perceptual spaces offers a promising avenue for future imagined speech BCIs.

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Multiple sequential prediction errors during reward processing in the human brain

Recent developments in reinforcement learning, cognitive control, and systems neuroscience highlight the complimentary roles in learning of valenced reward prediction errors (RPEs) and non-valenced salience prediction errors (PEs) driven by the magnitude of surprise. A core debate in reward learning focuses on whether valenced and non-valenced PEs can be isolated in the human electroencephalogram (EEG). Here, we combine behavioral modeling and single-trial EEG regression revealing a sequence of valenced and non-valenced PEs in an interval timing task dissociating outcome valence, magnitude, and probability. Multiple regression across temporal, spatial, and frequency dimensions revealed a spatio-tempo-spectral cascade from valenced RPE value represented by the feedback related negativity event-related potential (ERP) followed by non-valenced RPE magnitude and outcome probability effects indexed by subsequent P300 and late frontal positivity ERPs. The results show that learning is supported by a sequence of multiple PEs evident in the human EEG.

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Coupling between slow-waves and sharp-wave ripples organizes distributed neural activity during sleep in humans

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80-150 Hz) and subcortical/cortical slow-waves (0.5-4 Hz). However, the precise role of SWR-slow-wave interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, temporal and frontal cortices, to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high frequency activity (HFA; 70-200 Hz) a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical slow-waves. Finally, local cortical slow-wave phase offsets during SWRs predicted functional connectivity between the frontal and temporal cortex. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

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Intracranial recordings demonstrate medial temporal lobe engagement in visual search in humans

Visual search is a fundamental human behavior, which has been proposed to include two component processes: inefficient search (Search) and efficient search (Pop-out). According to extant research, these two processes map onto two separable neural systems located in the frontal and parietal association cortices. In the present study, we use intracranial recordings from 23 participants to delineate the neural correlates of Search and Pop-out with an unprecedented combination of spatiotemporal resolution and coverage across cortical and subcortical structures. First, we demonstrate a role for the medial temporal lobe in visual search, on par with engagement in frontal and parietal association cortex. Second, we show a gradient of increasing engagement over anatomical space from dorsal to ventral lateral frontal cortex. Third, we confirm previous work demonstrating nearly complete overlap in neural engagement across cortical regions in Search and Pop-out. We further demonstrate Pop-out selectivity manifesting as activity increase in Pop-out as compared to Search in a distributed set of sites including frontal cortex. This result is at odds with the view that Pop-out is implemented in low-level visual cortex or parietal cortex alone. Finally, we affirm a central role for the right lateral frontal cortex in Search.

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Slow wave-spindle coupling during sleep predicts language learning and associated oscillatory activity

Sentence comprehension involves the rapid decoding of both semantic and grammatical information, a process fundamental to communication. As with other complex cognitive processes, language comprehension relies, in part, on long-term memory. However, the electrophysiological mechanisms underpinning the initial encoding and generalisation of higher-order linguistic knowledge remain elusive, particularly from a sleep-based consolidation perspective. One candidate mechanism that may support the consolidation of higher-order language is the temporal coordination of slow oscillations (SO) and sleep spindles during non-rapid eye movement sleep (NREM). To examine this hypothesis, we analysed electroencephalographic (EEG) data recorded from 35 participants (Mage = 25.4, SD = 7.10; 16 males) during an artificial language learning task, contrasting performance between individuals who were given an 8hr nocturnal sleep period or an equivalent period of wake. We found that sleep relative to wake was associated with superior performance for rules that followed a sequence-based word order. Post-sleep sequence-based word order processing was further associated with less task-related theta desynchronisation, an electrophysiological signature of successful memory consolidation, as well as cognitive control and working memory. Frontal NREM SO-spindle coupling was also positively associated with behavioural sensitivity to sequence-based word order rules, as well as with task-related theta power. As such, theta activity during retrieval of previously learned information correlates with SO-spindle coupling, thus linking neural activity in the sleeping and waking brain. Taken together, this study presents converging behavioral and neurophysiological evidence for a role of NREM SO-spindle coupling and task-related theta activity as signatures of successful memory consolidation and retrieval in the context of higher-order language learning. SIGNIFICANCE STATEMENTThe endogenous temporal coordination of neural oscillations supports information processing during both wake and sleep states. Here we demonstrate that slow oscillation-spindle coupling during non-rapid eye movement sleep predicts the consolidation of complex grammatical rules and modulates task-related oscillatory dynamics previously implicated in sentence processing. We show that increases in theta power predict enhanced sensitivity to grammatical violations after a period of sleep and strong slow oscillation-spindle coupling modulates subsequent task-related theta activity to influence behaviour. Our findings reveal a complex interaction between both wake- and sleep-related oscillatory dynamics during the early stages of language learning beyond the single word level.

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Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study

Context modulates sensory neural activations enhancing perceptual and behavioral performance and reducing prediction errors. However, the mechanism of when and where these high-level expectations act on sensory processing is unclear. Here, we isolate the effect of expectation absent any auditory evoked activity by assessing the response to omitted expected sounds. Electrophysiological signals were recorded directly from the superior temporal gyrus (STG) and superior temporal sulcus (STS) in patients with medically refractory epilepsy. Subjects listened to a predictable sequence of syllables, with some infrequently omitted. We found a high frequency band (HFB, 70-150Hz) response to omissions, which overlap with a posterior subset of auditory active electrodes. This response is distinct from omission activations observed in non-auditory selective sites in STG. Heard syllables could be classified reliably from STG, but not the identity of the omitted stimulus. Both omission- and target detection activations were also observed in prefrontal cortex.\n\nWe propose that the posterior STG and STS are central for implementing predictions in the auditory environment. HFB omission activations in this region appear to index mismatch-signaling or salience detection processes.

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Electrocorticographic dissociation of alpha and beta rhythmic activity in the human sensorimotor system

This study uses electrocorticography in humans to assess how alpha- and beta-band rhythms modulate excitability of the sensorimotor cortex during movement selection, as indexed through a psychophysically-controlled movement imagery task. Both rhythms displayed effector-specific modulations, tracked spectral markers of action potentials in the local neuronal population, and showed spatially systematic phase relationships (traveling waves). Yet, alpha- and beta-band rhythms differed in their anatomical and functional properties, were weakly correlated, and traveled along opposite directions across the sensorimotor cortex. Increased alpha-band power in the somatosensory cortex ipsilateral to the selected arm was associated with spatially-unspecific inhibition. Decreased beta-band power over contralateral motor cortex was associated with a focal shift from relative inhibition to excitation. These observations indicate the relevance of both inhibition and disinhibition mechanisms for precise spatiotemporal coordination of neuronal populations during movement selection. Those mechanisms are implemented through the substantially different neurophysiological properties of sensorimotor alpha- and beta-band rhythms.

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An Electrophysiological Marker of Arousal Level in Humans

Deep non-rapid eye movement sleep (NREM) - also called slow wave sleep (SWS) - and general anesthesia are prominent states of reduced arousal linked to the occurrence of slow oscillations in the electroencephalogram (EEG). Rapid eye movement (REM) sleep, however, is also associated with a diminished arousal level, but is characterized by a desynchronized, wake-like EEG. This observation challenges the notion of oscillations as the main physiological mediator of reduced arousal. Using intracranial and surface EEG recordings in four independent data sets, we establish the 1/f spectral slope as an electrophysiological marker that accurately delineates wakefulness from anesthesia, SWS and REM sleep. The spectral slope reflects the non-oscillatory, scale-free measure of neural activity and has been proposed to index the local balance between excitation and inhibition. Taken together, these findings reconcile the long-standing paradox of reduced arousal in both REM and NREM sleep and provide a common unifying physiological principle -- a shift in local Excitation/ Inhibition balance -- to explain states of reduced arousal such as sleep and anesthesia in humans.\n\nSignificance StatementThe clinical assessment of arousal levels in humans depends on subjective measures such as responsiveness to verbal commands. While non-rapid eye movement (NREM) sleep and general anesthesia share some electrophysiological markers, rapid eye movement sleep (REM) is characterized by a wake-like electroencephalogram. Here, we demonstrate that non-oscillatory, scale-free electrical brain activity -- recorded from both scalp electroencephalogram and intracranial recordings in humans -- reliably tracks arousal levels during both NREM and REM sleep as well as under general anesthesia with propofol. Our findings suggest that non-oscillatory brain activity can be used effectively to monitor vigilance states.

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