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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

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

View PDF

Word pair classification during imagined speech using direct brain recordings

ABSTRACT

People that cannot communicate due to neurological disorders would bene t from an internal speech decoder. Here, we showed the ability to classify individual words during imagined speech from electrocorticographic signals. In a word imagery task, we used high gamma (70–150 Hz) time features with a support vector machine model to classify individual words from a pair of words. To account for temporal irregularities during speech production, we introduced a non-linear time alignment into the SVM kernel. Classi cation accuracy reached 88% in a two-class classi cation framework (50% chance level), and average classi cation accuracy across fteen word-pairs was signi cant across ve subjects (mean = 58%; p < 0.05). We also compared classi cation accuracy between imagined speech, overt speech and listening. As predicted, higher classi cation accuracy was obtained in the listening and overt speech conditions (mean = 89% and 86%, respectively; p < 0.0001), where speech stimuli were directly presented. The results provide evidence for a neural representation for imagined words in the temporal lobe, frontal lobe and sensorimotor cortex, consistent with previous ndings in speech perception and production. These data represent a proof of concept study for basic decoding of speech imagery, and delineate a number of key challenges to usage of speech imagery neural representations for clinical applications.

AUTHORS

• Stéphanie Martin

• Peter Brunner

• Iñaki Iturrate

• José del R. Millán

• Gerwin Schalk

• Robert T. Knight

• Brian Pasley

Date: 2016

DOI: 10.1038/srep25803

View PDF

Understanding and Decoding Thoughts in the Human Brain

ABSTRACT

Many people cannot communicate because of their physical problems, such as paralysis. These patients cannot speak with their friends, but their brains are still working well. They can think by themselves and would bene t from a device that could read their minds and translate their thoughts into audible speech. In our study, we placed electrodes beneath patients’ skulls, directly at the surface of the brain, and measured brain activity while the patients were thinking. We then tried to decode and translate the words that they imagined into audible sounds. We showed that we could decode some parts of the sound of what patients were thinking. This was our rst attempt at translating thoughts to speech, and we hope to get much better, as many patients who cannot speak but have thoughts in their minds could bene t from a “speech decoder.”

AUTHORS

• Stéphanie Martin

• Christian Mikutta

• Robert T. Knight

• Brian Pasley

Date: 2016

DOI: 10.3389/frym.2016.00004

View PDF

Behavioral and EEG Evidence for Auditory Memory Suppression

ABSTRACT

The neural basis of motivated forgetting using the Think/No-Think (TNT) paradigm is receiving increased attention with a particular focus on the mechanisms that enable memory suppression. However, most TNT studies have been limited to the visual domain. To assess whether and to what extent direct memory suppression extends across sensory modalities, we examined behavioral and electroencephalographic (EEG) effects of auditory TNT in healthy young adults by adapting the TNT paradigm to the auditory modality. Behaviorally, suppression of memory strength was indexed by prolonged response time (RTs) during the retrieval of subsequently remembered No-Think words. We examined task-related EEG activity of both attempted memory retrieval and inhibition of a previously learned target word during the presentation of its paired associate. Event-related EEG responses revealed two main findings: (1) a centralized Think > No-Think positivity during auditory word presentation (from approximately 0–500 ms); and (2) a sustained Think positivity over parietal electrodes beginning at approximately 600 ms reflecting the memory retrieval effect which was significantly reduced for No-Think words. In addition, word-locked theta (4–8 Hz) power was initially greater for No-Think compared to Think during auditory word presentation over fronto-central electrodes. This was followed by a posterior theta increase indexing successful memory retrieval in the Think condition. The observed event-related potential pattern and theta power analysis are similar to that reported in visual TNT studies and support a modality non-specific mechanism for memory inhibition. The EEG data also provide evidence supporting differing roles and time courses of frontal and parietal regions in the flexible control of auditory memory.

AUTHORS

• Maya Cano

• Robert T. Knight

Date: 2016

DOI: 10.3389/fnhum.2016.00133

View PDF

A Cool Approach to Probing Speech Cortex

ABSTRACT

In this issue of Neuron, Long et al. (2016) employ a novel technique of intraoperative cortical cooling in humans during speech production. They demonstrate that cooling Broca’s area interferes with speech timing but not speech quality.

AUTHORS

• Adeen Flinker

• Robert T. Knight

Date: 2016

DOI: 10.1016/j.neuron.2016.02.039

View PDF

Extracting duration information in a picture category decoding task using Hidden Markov Models

ABSTRACT

Adapting classifiers for the purpose of brain signal decoding is a major challenge in brain–computer-interface (BCI) research. In a previous study we showed in principle that hidden Markov models (HMM) are a suitable alternative to the well-studied static classifiers. However, since we investigated a rather straightforward task, advantages from modeling of the signal could not be assessed. Approach. Here, we investigate a more complex data set in order to find out to what extent HMMs, as a dynamic classifier, can provide useful additional information. We show for a visual decoding problem that besides category information, HMMs can simultaneously decode picture duration without an additional training required. This decoding is based on a strong correlation that we found between picture duration and the behavior of the Viterbi paths. Main results. Decoding accuracies of up to 80% could be obtained for category and duration decoding with a single classifier trained on category information only. Significance. The extraction of multiple types of information using a single classifier enables the processing of more complex problems, while preserving good training results even on small databases. Therefore, it provides a convenient framework for online real-life BCI utilizations.

AUTHORS

• Tim Pfeiffer

• Nicolai Heinze

• Robert Frysch

• Leon Y. Deouell

• Mircea Schoenfeld

• Robert T. Knight

• Georg Rose

Date: 2016

DOI: doi:10.1088/1741-2560/13/2/026010

View PDF

Choosing words: left hemisphere, right hemisphere, or both? Perspective on the lateralization of word retrieval

ABSTRACT

Language is considered to be one of the most lateralized human brain functions. Left hemisphere dominance for language has been consistently confirmed in clinical and experimental settings and constitutes one of the main axioms of neurology and neuroscience. However, functional neuroimaging studies are finding that the right hemisphere also plays a role in diverse language functions. Critically, the right hemisphere may also compensate for the loss or degradation of language functions following extensive stroke-induced damage to the left hemisphere. Here, we review studies that focus on our ability to choose words as we speak. Although fluidly performed in individuals with intact language, this process is routinely compromised in aphasic patients. We suggest that parceling word retrieval into its subprocesses—lexical activation and lexical selection—and examining which of these can be compensated for after left hemisphere stroke can advance the understanding of the lateralization of word retrieval in speech production. In particular, the domain-general nature of the brain regions associated with each process may be a helpful indicator of the right hemisphere’s propensity for compensation.

AUTHORS

• Stephanie Ries

• Nina F. Dronkers

• Robert T. Knight

Date: 2016

View PDF