Bidirectional frontoparietal oscillatory systems support working memory

ABSTRACT

The ability to represent and select information in working memory provides the neurobiological infrastructure for human cognition. For 80 years, dominant views of working memory have focused on the key role of prefrontal cortex (PFC). However, more recent work has implicated posterior cortical regions, suggesting that PFC engagement during working memory is dependent on the degree of executive demand. We provide evidence from neurological patients with discrete PFC damage that challenges the dominant models attributing working memory to PFC-dependent systems. We show that neural oscillations, which provide a mechanism for PFC to communicate with posterior cortical regions, independently subserve communications both to and from PFC—uncovering parallel oscillatory mechanisms for working memory. Fourteen PFC patients and 20 healthy, age-matched controls performed a working memory task where they encoded, maintained, and actively processed information about pairs of common shapes. In controls, the electroencephalogram (EEG) exhibited oscillatory activity in the low-theta range over PFC and directional connectivity from PFC to parieto-occipital regions commensurate with executive processing demands. Concurrent alpha-beta oscillations were observed over parieto-occipital regions, with directional connectivity from parieto-occipital regions to PFC, regardless of processing demands. Accuracy, PFC low-theta activity, and PFC / parieto-occipital connectivity were attenuated in patients, revealing a PFC-independent, alpha-beta system. The PFC patients still demonstrated task proficiency, which indicates that the posterior alpha-beta system provides sufficient resources for working memory. Taken together, our findings reveal neurologically dissociable PFC and parieto-occipital systems and suggest that parallel, bidirectional oscillatory systems form the basis of working memory.

AUTHORS

• Elizabeth L. Johnson

• Callum Dewar

• Anne-Kristin Solbakk

• Tor Endestad

• Torstein Meling

• Robert T. Knight

Date: 2017

DOI: 10.1016/j.cub.2017.05.046

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Neuroplasticity of language in left-hemisphere stroke: evidence linking subsecond electrophysiology and structural connections

ABSTRACT

The understanding of neuroplasticity following stroke is predominantly based on neuroimaging measures that cannot address the subsecond neurodynamics of impaired language processing. We combined behavioral and electrophysiological measures and structural-connectivity estimates to characterize neuroplasticity underlying successful compensation of language abilities after left-hemispheric stroke. We recorded the electroencephalogram from patients with stroke lesions to the left temporal lobe and from matched controls during context-driven word retrieval. Participants heard lead-in sentences that either constrained the final word (“He locked the door with the”) or not (“She walked in here with the”). The last word was shown as a picture to be named. Individual-participant analyses were conducted, focusing on oscillatory power as a subsecond indicator of a brain region’s functional neurophysiological computations. All participants named pictures faster following constrained than unconstrained sentences, except for two patients, who had extensive damage to the left temporal lobe. Left-lateralized alpha–beta oscillatory power decreased in controls pre-picture presentation for constrained relative to unconstrained contexts. In patients, the alpha–beta power decreases were observed with the same time course as in controls but were lateralized to the intact right hemisphere. The right lateralization depended on the probability of white-matter connections between the bilateral temporal lobes. The two patients who performed poorly behaviorally showed no alpha–beta power decreases. Our findings suggest that incorporating direct measures of neural activity into investigations of neuroplasticity can provide important neural markers to help predict language recovery, assess the progress of neurorehabilitation, and delineate targets for therapeutic neuromodulation.

AUTHORS

• Vitoria Piai

• Lars Meyer

• Nina F. Dronkers

• Robert T. Knight

Date: 2017

DOI: 10.1002/hbm.23581

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Instantaneous voltage as an alternative to power- and phase-based interpretation of oscillatory brain activity

Abstract

For decades, oscillatory brain activity has been characterized primarily by measurements of power and phase. While many studies have linked those measurements to cortical excitability, their relationship to each other and to the physiological underpinnings of excitability is unclear. The recently proposed Function-through-Biased- Oscillations (FBO) hypothesis (Schalk, 2015) addressed these issues by suggesting that the voltage potential at the cortical surface directly reflects the excitability of cortical populations, that this voltage is rhythmically driven away from a low resting potential (associated with depolarized cortical populations) towards positivity (associated with hyperpolarized cortical populations). This view explains how oscillatory power and phase together influence the instantaneous voltage potential that directly regulates cortical excitability. This implies that the alternative measurement of instantaneous voltage of oscillatory activity should better predict cortical excitability compared to either of the more traditional measurements of power or phase. Using electrocorticographic (ECoG) data from 28 human subjects, the results of our study confirm this prediction: compared to oscillatory power and phase, the instantaneous voltage explained 20% and 31% more of the variance in broadband gamma, respectively, and power and phase together did not produce better predictions than the instantaneous voltage. These results synthesize the previously separate power- and phase-based interpretations and associate oscillatory activity directly with a physiological interpretation of cortical excitability. This alternative view has implications for the interpretation of studies of oscillatory activity and for current theories of cortical information transmission.

Authors

• Gerwin Schalk

• Joshua Marple

• Robert T. Knight

• William G. Coon

Date: 2017

DOI: 10.1016/j.neuroimage.2017.06.01

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Spatiotemporal dynamics of word retrieval in speech production revealed by cortical high-frequency band activity

ABSTRACT

Word retrieval is core to language production and relies on complementary processes: the rapid activation of lexical and conceptual representations and word selection, which chooses the correct word among semantically related competitors. Lexical and conceptual activation is measured by semantic priming. In contrast, word selection is indexed by semantic interference and is hampered in semantically homogeneous (HOM) contexts. We examined the spatiotemporal dynamics of these complementary processes in a picture naming task with blocks of semantically heterogeneous (HET) or HOM stimuli. We used electrocorticography data obtained from frontal and temporal cortices, permitting detailed spatiotemporal analysis of word retrieval processes. A semantic interference effect was observed with naming latencies longer in HOM versus HET blocks. Cortical response strength as indexed by high-frequency band (HFB) activity (70–150 Hz) amplitude revealed effects linked to lexical-semantic activation and word selection observed in widespread regions of the cortical mantle. Depending on the subsecond timing and cortical region, HFB indexed semantic interference (i.e., more activity in HOM than HET blocks) or semantic priming effects (i.e., more activity in HET than HOM blocks). These effects overlapped in time and space in the left posterior inferior temporal gyrus and the left prefrontal cortex. The data do not support a modular view of word retrieval in speech production but rather support substantial overlap of lexical-semantic activation and word selection mechanisms in the brain.

AUTHORS

• Stephanie Ries

• Rhummit K. Dhillon

• Alex Clarke

• David King-Stephens

• Kenneth Laxer

• Peter Weber

• Rachel A. Kuperman

• Kurtis I. Auguste

• Peter Brunner

• Gerwin Schalk

• Jack J. Lin

• Josef Parvizi

• Nathan E. Crone

• Nina F. Dronkers

• Robert T. Knight

Date: 2017

DOI: 10.1073/pnas.1620669114

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Effects of prefrontal cortex damage on emotion understanding: EEG and behavioural evidence

ABSTRACT

Humans are highly social beings that interact with each other on a daily basis. In these complex interactions, we get along by being able to identify others’ actions and infer their intentions, thoughts and feelings. One of the major theories accounting for this critical ability assumes that the understanding of social signals is based on a primordial tendency to simulate observed actions by activating a mirror neuron system. If mirror neuron regions are important for action and emotion recognition, damage to regions in this network should lead to deficits in these domains. In the current behavioural and EEG study, we focused on the lateral prefrontal cortex including dorsal and ventral prefrontal cortex and utilized a series of task paradigms, each measuring a different aspect of recognizing others’ actions or emotions from body cues. We examined 17 patients with lesions including (n = 8) or not including (n = 9) the inferior frontal gyrus, a core mirror neuron system region, and compared their performance to matched healthy control subjects (n = 18), in behavioural tasks and in an EEG observation—execution task measuring mu suppression. Our results provide support for the role of the lateral prefrontal cortex in understanding others’ emotions, by showing that even unilateral lesions result in deficits in both accuracy and reaction time in tasks involving the recognition of others’ emotions. In tasks involving the recognition of actions, patients showed a general increase in reaction time, but not a reduction in accuracy. Deficits in emotion recognition can be seen by either direct damage to the inferior frontal gyrus, or via damage to dorsal lateral prefrontal cortex regions, resulting in deteriorated performance and less EEG mu suppression over sensorimotor cortex.

AUTHORS

• Anat Perry

• Samantha N. Saunders

• Jennifer Stiso

• Callum Dewar

• James Lubell

• Torstein Meling

• Anne-Kristin Solbakk

• Tor Endestad

• Robert T. Knight

Date: 2017

DOI: 10.1093/brain/awx031

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Amygdala-hippocampal dynamics during salient information processing

ABSTRACT

Recognizing motivationally salient information is critical to guiding behaviour. The amygdala and hippocampus are thought to support this operation, but the circuit-level mechanism of this interaction is unclear. We used direct recordings in the amygdala and hippocampus from human epilepsy patients to examine oscillatory activity during processing of fearful faces compared with neutral landscapes. We report high gamma (70–180 Hz) activation for fearful faces with earlier stimulus evoked onset in the amygdala compared with the hippocampus. Attending to fearful faces compared with neutral landscape stimuli enhances low-frequency coupling between the amygdala and the hippocampus. The interaction between the amygdala and hippocampus is largely unidirectional, with theta/alpha oscillations in the amygdala modulating hippocampal gamma activity. Granger prediction, phase slope index and phase lag analysis corroborate this directional coupling. These results demonstrate that processing emotionally salient events in humans engages an amygdala-hippocampal network, with the amygdala influencing hippocampal dynamics during fear processing.

AUTHORS

• Robert T. Knight

• Avgusta Shestyuk

• Kristopher L. Anderson

• Jie Zheng

• Stephanie L. Leal

• Gultekin Gulsen

• Lilit Mnatsakanyan

• Sumeet Vadera

• Frank P.K. Hsu

• Michael A. Yassa

• Jack J. Lin

Date: 2017

DOI: 10.1038/ncomms14413

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Bringing Kids into the Scientific Review Process

ABSTRACT

Frontiers for Young Minds puts kids in charge of scientific publications by having them control the review process. This provides kids the ability to shape the way science is taught and to better understand the scientific method.

AUTHORS

• Robert T. Knight

• Sabine Kastner

Date: 2017

DOI: http://dx.doi.org/10.1016/j.neuron.2016.12.002

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Rapid tuning shifts in human auditory cortex enhance speech intelligibility

ABSTRACT

Experience shapes our perception of the world on a moment-to-moment basis. This robust perceptual effect of experience parallels a change in the neural representation of stimulus features, though the nature of this representation and its plasticity are not well-understood. Spectrotemporal receptive field (STRF) mapping describes the neural response to acoustic features, and has been used to study contextual effects on auditory receptive fields in animal models. We performed a STRF plasticity analysis on electrophysiological data from recordings obtained directly from the human auditory cortex. Here, we report rapid, automatic plasticity of the spectrotemporal response of recorded neural ensembles, driven by previous experience with acoustic and linguistic information, and with a neurophysiological effect in the sub-second range. This plasticity reflects increased sensitivity to spectrotemporal features, enhancing the extraction of more speech-like features from a degraded stimulus and providing the physiological basis for the observed ‘perceptual enhancement’ in understanding speech.

AUTHORS

• Chris Holdgraf

• Wendy de Heer

• Brian Pasley

• Jochem W. Rieger

• Nathan E. Crone

• Jack J. Lin

• Robert T. Knight

• Frédéric E. Theunissen

Date: 2016

DOI: 10.1038/ncomms13654

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Non-sinusoidal activity can produce cross-frequency coupling in cortical signals in the absence of functional interaction between neural sources

ABSTRACT

The analysis of cross-frequency coupling (CFC) has become popular in studies involving intracranial and scalp EEG recordings in humans. It has been argued that some cases where CFC is mathematically present may not reflect an interaction of two distinct yet functionally coupled neural sources with different frequencies. Here we provide two empirical examples from intracranial recordings where CFC can be shown to be driven by the shape of a periodic waveform rather than by a functional interaction between distinct sources. Using simulations, we also present a generalized and realistic scenario where such coupling may arise. This scenario, which we term waveform-dependent CFC, arises when sharp waveforms (e.g., cortical potentials) occur throughout parts of the data, in particular if they occur rhythmically. Since the waveforms contain both low- and high-frequency components, these components can be inherently phase-aligned as long as the waveforms are spaced with appropriate intervals. We submit that such behavior of the data, which seems to be present in various cortical signals, cannot be interpreted as reflecting functional modulation between distinct neural sources without additional evidence. In addition, we show that even low amplitude periodic potentials that cannot be readily observed or controlled for, are sufficient for significant CFC to occur.

AUTHORS

• Edden Gerber

• Boaz Sadeh

• Andrew Ward

• Robert T. Knight

• Leon Y. Deouell

Date: 2016

DOI: 10.1371/journal.pone.0167351

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Oscillatory Dynamics of Prefrontal Cognitive Control

ABSTRACT

The prefrontal cortex (PFC) provides the structural basis for numerous higher cognitive functions. However, it is still largely unknown which mechanisms provide the functional basis for flexible cognitive control of goal-directed behavior. Here, we review recent findings that suggest that the functional architecture of cognition is profoundly rhythmic and propose that the PFC serves as a conductor to orchestrate task-relevant large-scale networks. We highlight several studies that demonstrated that oscillatory dynamics, such as phase resetting, cross-frequency coupling (CFC), and entrainment, support PFC-dependent recruitment of task-relevant regions into coherent functional networks. Importantly, these findings support the notion that distinct spectral signatures reflect different cortical computations supporting effective multiplexing on different temporal channels along the same anatomical pathways.

AUTHORS

• Randolph Helfrich

• Robert T. Knight

Date: 2016

DOI: dx.doi.org/10.1016/j.tics.2016.09.007

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Differential Sources for 2 Neural Signatures of Target Detection: An Electrocorticography Study

ABSTRACT

Electrophysiology and neuroimaging provide conflicting evidence for the neural contributions to target detection. Scalp electroencephalography (EEG) studies localize the P3b event-related potential component mainly to parietal cortex, whereas neuroimaging studies report activations in both frontal and parietal cortices. We addressed this discrepancy by examining the sources that generate the target-detection process using electrocorticography (ECoG). We recorded ECoG activity from cortex in 14 patients undergoing epilepsy monitoring, as they performed an auditory or visual target-detection task. We examined target-related responses in 2 domains: high frequency band (HFB) activity and the P3b. Across tasks, we observed a greater proportion of electrodes that showed target-specific HFB power relative to P3b over frontal cortex, but their proportions over parietal cortex were comparable. Notably, there was minimal overlap in the electrodes that showed target-specific HFB and P3b activity. These results revealed that the target-detection process is characterized by at least 2 different neural markers with distinct cortical distributions. Our findings suggest that separate neural mechanisms are driving the differential patterns of activity observed in scalp EEG and neuroimaging studies, with the P3b reflecting EEG findings and HFB activity reflecting neuroimaging findings, highlighting the notion that target detection is not a unitary phenomenon.

AUTHORS

• Julia W. Y. Kam

• Sara Szczepanski

• Ryan T. Canolty

• Adeen Flinker

• Kurtis I. Auguste

• Nathan E. Crone

• Heidi E. Kirsch

• Rachel A. Kuperman

• Jack J. Lin

• Josef Parvizi

• Robert T. Knight

Date: 2016

DOI: 10.1093/cercor/bhw343

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Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones

ABSTRACT

Objective Ripples (80–150 Hz) recorded from clinical macroelectrodes have been shown to be an accurate biomarker of epileptogenic brain tissue. We investigated coupling between epileptiform spike phase and ripple amplitude to better understand the mechanisms that generate this type of pathologic ripple (pRipple) event. Methods We quantified phase amplitude coupling (PAC) between epileptiform electroencephalography (EEG) spike phase and ripple amplitude recorded from intracranial depth macroelectrodes during episodes of sleep in 12 patients with mesial temporal lobe epilepsy. PAC was determined by (1) a phasor transform that corresponds to the strength and rate of ripples coupled with spikes, and a (2) ripple-triggered average to measure the strength, morphology, and spectral frequency of the modulating and modulated signals. Coupling strength was evaluated in relation to recording sites within and outside the seizure-onset zone (SOZ). Results Both the phasor transform and ripple-triggered averaging methods showed that ripple amplitude was often robustly coupled with epileptiform EEG spike phase. Coupling was found more regularly inside than outside the SOZ, and coupling strength correlated with the likelihood a macroelectrode's location was within the SOZ (p < 0.01). The ratio of the rate of ripples coupled with EEG spikes inside the SOZ to rates of coupled ripples in non-SOZ was greater than the ratio of rates of ripples on spikes detected irrespective of coupling (p < 0.05). Coupling strength correlated with an increase in mean normalized ripple amplitude (p < 0.01), and a decrease in mean ripple spectral frequency (p < 0.05). Significance Generation of low-frequency (80–150 Hz) pRipples in the SOZ involves coupling between epileptiform spike phase and ripple amplitude. The changes in excitability reflected as epileptiform spikes may also cause clusters of pathologically interconnected bursting neurons to grow and synchronize into aberrantly large neuronal assemblies.

AUTHORS

• Shennan A. Weiss

• Iren Orosz

• Noriko Salamon

• Stephanie Moy

• Linqing Wei

• Maryse A. Van't Klooster

• Robert T. Knight

• Ronald M. Harper

• Anatol Bragin

• Itzhak Fried

• Jerome Engel Jr.

• Richard J. Staba

Date: 2016

DOI: 10.1111/epi.13572

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Direct brain recordings reveal hippocampal rhythm underpinnings of language processing

ABSTRACT

Language is classically thought to be supported by perisylvian cortical regions. Here we provide intracranial evidence linking the hippocampal complex to linguistic processing. We used direct recordings from the hippocampal structures to investigate whether theta oscillations, pivotal in memory function, track the amount of contextual linguistic information provided in sentences. Twelve participants heard sentences that were either constrained (“She locked the door with the”) or unconstrained (“She walked in here with the”) before presentation of the final word (“key”), shown as a picture that participants had to name. Hippocampal theta power increased for constrained relative to unconstrained contexts during sentence processing, preceding picture presentation. Our study implicates hippocampal theta oscillations in a language task using natural language associations that do not require memorization. These findings reveal that the hippocampal complex contributes to language in an active fashion, relating incoming words to stored semantic knowledge, a necessary process in the generation of sentence meaning.

AUTHORS

• Vitoria Piai

• Kristopher L. Anderson

• Jack J. Lin

• Callum Dewar

• Josef Parvizi

• Nina F. Dronkers

• Robert T. Knight

Date: 2016

DOI: www.pnas.org/cgi/doi/10.1073/pnas.1603312113

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Atypical brain mechanisms of prediction according to uncertainty in autism

ABSTRACT

Resistance to change is often reported in autism and may arise from an inability to predict events in uncertain contexts. Using EEG recorded in 12 adults with autism and age-matched controls performing a visual target detection task, we characterized the influence of a certain context (targets preceded by a predictive sequence of three distinct stimuli) or an uncertain context (random targets) on behavior and electrophysiological markers of predictive processing. During an uncertain context, adults with autism were faster than controls to detect targets. They also had an enhancement in CNV amplitude preceding all random stimuli—indexing enhanced preparatory mechanisms, and an earlier N2 to targets—reflecting faster information processing—compared to controls. During a certain context, both controls and adults with autism presented an increase in P3 amplitude to predictive stimuli—indexing information encoding of the predictive sequence, an enhancement in CNV amplitude preceding predictable targets—corresponding to the deployment of preparatory mechanisms, and an earlier P3 to predictable targets—reflecting efficient prediction building and implementation. These results suggest an efficient extraction of predictive information to generate predictions in both controls and adults with autism during a certain context. However, adults with autism displayed a failure to decrease mu power during motor preparation accompanied by a reduced benefit in reaction times to predictable targets. The data reveal that patients with autism over-anticipate stimuli occurring in an uncertain context, in accord with their sense of being overwhelmed by incoming information. These results suggest that adults with autism cannot flexibly modulate cortical activity according to changing levels of uncertainty.

AUTHORS

• Alix Thillay

• Mathieu Lemaire

• S. Roux

• Emmanuelle Houy-Durand

• C. Barthelemy

• Robert T. Knight

• Aurélie Bidet-Caulet

• Frederique Bonnet-Brilhault

Date: 2016

DOI: 10.3389/fnins.2016.00317

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The role of the orbitofrontal cortex in regulation of interpersonal space: evidence from frontal lesion and frontotemporal dementia patients

ABSTRACT

Interpersonal distance is central to communication and complex social behaviors but the neural correlates of interpersonal distance preferences are not defined. Previous studies suggest that damage to the orbitofrontal cortex (OFC) is associated with impaired interpersonal behavior. To examine whether the OFC is critical for maintaining appropriate interpersonal distance, we tested two groups of patients with OFC damage: Patients with OFC lesions and patients with behavioral variant frontotemporal dementia. These two groups were compared to healthy controls and to patients with lesions restricted to the dorsolateral prefrontal cortex. Only patients with OFC damage showed abnormal interpersonal distance preferences, which were significantly different from both controls and patients with dorsolateral prefrontal damage. The comfortable distances these patients chose with strangers were significantly closer than the other groups and resembled distances normally used with close others. These results shed light on the role of the OFC in regulating social behavior and may serve as a simple diagnostic tool for dementia or lesion patients.

AUTHORS

• Anat Perry

• Sandy J. Lwi

• Alice Verstaen

• Callum Dewar

• Robert W. Levenson

• Robert T. Knight

Date: 2016

DOI: 10.1093/scan/nsw109

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Frontal monitoring and parietal evidence: mechanisms of error correction

ABSTRACT

When we respond to a stimulus, our decisions are based not only on external stimuli but also on our ongoing performance. If the response deviates from our goals, monitoring and decision-making brain areas interact so that future behavior may change. By taking advantage of natural variation in error salience, as measured by the RT taken to correct an error (RTEC), here we argue that an evidence accumulation framework provides a potential underlying mechanism for this variable process of error identification and correction, as evidenced by covariation of frontal monitoring and parietal decision-making processes. We study two early EEG signals linked to monitoring within medial PFC—the error-related negativity (ERN) and frontocentral theta activity—and a third EEG signal, the error positivity (Pe), that is thought to share the same parietal substrates as a signal (the P3b) proposed to reflect evidence accumulation. As predicted, our data show that on slow RTEC trials, frontal monitoring resources are less strongly employed, and the latency of the Pe is longer. Critically, the speed of the RTEC also covaries with the magnitude of subsequent neural (intertrial alpha power) and behavioral (post-error slowing) adjustments following the correction. These results are synthesized to describe a timing diagram for adaptive decision-making after errors and support a potential evidence accumulation mechanism in which error signaling is followed by rapid behavioral adjustments.

AUTHORS

• Ana Navarro-Cebrian

• Robert T. Knight

• Andrew S. Kayser

Date: 2016

DOI: 10.1162/jocn_a_00962

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ERP Correlates of Proactive and Reactive Cognitive Control in Treatment-Naïve Adult ADHD

ABSTRACT

This study investigated whether treatment naïve adults with Attention Deficit Hyperactivity Disorder (ADHD; n = 33; 19 female) differed from healthy controls (n = 31; 17 female) in behavioral performance, event-related potential (ERP) indices of preparatory attention (CueP3 and late CNV), and reactive response control (Go P3, NoGo N2, and NoGo P3) derived from a visual cued Go/NoGo task. On several critical measures, Cue P3, late CNV, and NoGo N2, there were no significant differences between the groups. This indicated normal preparatory processes and conflict monitoring in ADHD patients. However, the patients had attenuated Go P3 and NoGoP3 amplitudes relative to controls, suggesting reduced allocation of attentional resources to processes involved in response control. The patients also had a higher rate of Go signal omission errors, but no other performance decrements compared with controls. Reduced Go P3 and NoGo P3 amplitudes were associated with poorer task performance, particularly in the ADHD group. Notably, the ERPs were not associated with self-reported mood or anxiety. The results provide electrophysiological evidence for reduced effortful engagement of attentional resources to both Go and NoGo signals when reactive response control is needed. The absence of group differences in ERP components indexing proactive control points to impairments in specific aspects of cognitive processes in an untreated adult ADHD cohort. The associations between ERPs and task performance provided additional support for the altered electrophysiological responses.

AUTHORS

• Venke A. Grane

• Jan F. Brunner

• Tor Endestad

• Ida E.S. Aasen

• Juri Kropotov

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2016

DOI: 10.1371/journal.pone.0159833

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The use of intracranial recordings to decode human language: Challenges and opportunities

ABSTRACT

Decoding speech from intracranial recordings serves two main purposes: understanding the neural correlates of speech processing and decoding speech features for targeting speech neuroprosthetic devices. Intracranial recordings have high spatial and temporal resolution, and thus offer a unique opportunity to investigate and decode the electrophysiological dynamics underlying speech processing. In this review article, we describe current approaches to decoding different features of speech perception and production – such as spectrotemporal, phonetic, phonotactic, semantic, and articulatory components – using intracranial recordings. A specific section is devoted to the decoding of imagined speech, and potential applications to speech prosthetic devices. We outline the challenges in decoding human language, as well as the opportunities in scientific and neuroengineering applications.

AUTHORS

• Stéphanie Martin

• José del R. Millán

• Robert T. Knight

• Brian Pasley

Date: 2016

DOI: 10.1016/j.bandl.2016.06.003

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Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

ABSTRACT

Predictive coding theories posit that neural networks learn statistical regularities in the environment for comparison with actual outcomes, signaling a prediction error (PE) when sensory deviation occurs. PE studies in audition have capitalized on low-frequency event-related potentials (LF-ERPs), such as the mismatch negativity. However, local cortical activity is well-indexed by higher-frequency bands [high-γ band (Hγ): 80–150 Hz]. We compared patterns of human Hγ and LF-ERPs in deviance detection using electrocorticographic recordings from subdural electrodes over frontal and temporal cortices. Patients listened to trains of task-irrelevant tones in two conditions differing in the predictability of a deviation from repetitive background stimuli (fully predictable vs. unpredictable deviants). We found deviance-related responses in both frequency bands over lateral temporal and inferior frontal cortex, with an earlier latency for Hγ than for LF-ERPs. Critically, frontal Hγ activity but not LF-ERPs discriminated between fully predictable and unpredictable changes, with frontal cortex sensitive to unpredictable events. The results highlight the role of frontal cortex and Hγ activity in deviance detection and PE generation.

AUTHORS

• S. Durschmid

• Erik Edwards

• Christoph Reichert

• Callum Dewar

• Hermann Hinrichs

• Hans-Jochen Heinze

• Heidi E. Kirsch

• Sarang S. Dalal

• Leon Y. Deouell

• Robert T. Knight

Date: 2016

DOI: 10.1073/pnas.1525030113

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Pre-stimulus thalamic theta power predicts human memory formation

ABSTRACT

Pre-stimulus theta (4–8 Hz) power in the hippocampus and neocortex predicts whether a memory for a subsequent event will be formed. Anatomical studies reveal thalamus-hippocampal connectivity, and lesion, neuroimaging, and electrophysiological studies show that memory processing involves the dorsomedial (DMTN) and anterior thalamic nuclei (ATN). The small size and deep location of these nuclei have limited real-time study of their activity, however, and it is unknown whether pre-stimulus theta power predictive of successful memory formation is also found in these subcortical structures. We recorded human electrophysiological data from the DMTN and ATN of 7 patients receiving deep brain stimulation for refractory epilepsy. We found that greater pre-stimulus theta power in the right DMTN was associated with successful memory encoding, predicting both behavioral outcome and post-stimulus correlates of successful memory formation. In particular, significant correlations were observed between right DMTN theta power and both frontal theta and right ATN gamma (32–50 Hz) phase alignment, and frontal-ATN theta-gamma cross-frequency coupling. We draw the following primary conclusions. Our results provide direct electrophysiological evidence in humans of a role for the DMTN as well as the ATN in memory formation. Furthermore, prediction of subsequent memory performance by pre-stimulus thalamic oscillations provides evidence that post-stimulus differences in thalamic activity that index successful and unsuccessful encoding reflect brain processes specifically underpinning memory formation. Finally, the findings broaden the understanding of brain states that facilitate memory encoding to include subcortical as well as cortical structures.

AUTHORS

• Catherine M. Sweeney-Reed

• Tino Zaehle

• Jürgen Voges

• Friedhelm Schmitt

• Lars Buentjen

• Klaus Kopitzki

• Alan Richardson-Klavehn

• Hermann Hinrichs

• Hans-Jochen Heinze

• Robert T. Knight

• Michael D. Rugg

Date: 2016

DOI: 10.1016/j.neuroimage.2016.05.042

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