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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Cortical Spatio-temporal Dynamics Underlying Phonological Target Detection in Humans

Authors:

• Edward F. Chang

• Erik Edwards

• Srikantan S. Nagarajan

• Noa Fogelson

• Sarang S. Dalal

• Ryan T. Canolty

• Heidi E. Kirsch

• Nicholas M. Barbaro

• Robert T. Knight

Date: 2011

DOI: 10.1162/jocn.2010.21466

PubMed: 20465359

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Abstract:

Selective processing of task-relevant stimuli is critical for goal-directed behavior. We used electrocorticography to assess the spatio-temporal dynamics of cortical activation during a simple phonological target detection task, in which subjects press a button when a prespecified target syllable sound is heard. Simultaneous surface potential recordings during this task revealed a highly ordered temporal progression of high gamma (HG, 70-200 Hz) activity across the lateral hemisphere in less than 1 sec. The sequence demonstrated concurrent regional sensory processing of speech syllables in the posterior superior temporal gyrus (STG) and speech motor cortex, and then transitioned to sequential task-dependent processing from prefrontal cortex (PFC), to the final motor response in the hand sensorimotor cortex. STG activation was modestly enhanced for target over nontarget sounds, supporting a selective gain mechanism in early sensory processing, whereas PFC was entirely selective to targets, supporting its role in guiding response behavior. These results reveal that target detection is not a single cognitive event, but rather a process of progressive target selectivity that involves large-scale rapid parallel and serial processing in sensory, cognitive, and motor structures to support goal-directed human behavior.

Spatiotemporal imaging of cortical activation during verb generation and picture naming

Authors:

• Erik Edwards

• Srikantan S. Nagarajan

• Sarang S. Dalal

• Ryan T. Canolty

• Heidi E. Kirsch

• Nicholas M. Barbaro

• Robert T. Knight

Date: 2010

DOI: 10.1016/j.neuroimage.2009.12.035.

PubMed: 20026224

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Abstract:

One hundred and fifty years of neurolinguistic research has identified the key structures in the human brain that support language. However, neither the classic neuropsychological approaches introduced by Broca (1861) and Wernicke (1874), nor modern neuroimaging employing PET and fMRI has been able to delineate the temporal flow of language processing in the human brain. We recorded the electrocorticogram (ECoG) from indwelling electrodes over left hemisphere language cortices during two common language tasks, verb generation and picture naming. We observed that the very high frequencies of the ECoG (high-gamma, 70–160 Hz) track language processing with spatial and temporal precision. Serial progression of activations is seen at a larger timescale, showing distinct stages of perception, semantic association/selection, and speech production. Within the areas supporting each of these larger processing stages, parallel (or “incremental”) processing is observed. In addition to the traditional posterior vs. anterior localization for speech perception vs. production, we provide novel evidence for the role of premotor cortex in speech perception and of Wernicke’s and surrounding cortex in speech production. The data are discussed with regards to current leading models of speech perception and production, and a “dual ventral stream” hybrid of leading speech perception models is given.

Cortical spatiotemporal dynamics underlying phonological target detection in humans

Authors:

• Edward F. Chang

• Erik Edwards

• Srikantan S. Nagarajan

• Noa Fogelson

• Sarang S. Dalal

• Ryan T. Canolty

• Heidi E. Kirsch

• Nicholas M. Barbaro

• Robert T. Knight

Date: 2010

DOI: 10.1162/jocn.2010.21466

PubMed: 20465359

View PDF

Abstract:

Selective processing of task-relevant stimuli is critical for goal-directed behavior. We used electrocorticography to assess the spatio-temporal dynamics of cortical activation during a simple phonological target detection task, in which subjects press a button when a prespecified target syllable sound is heard. Simultaneous surface potential recordings during this task revealed a highly ordered temporal progression of high gamma (HG, 70–200 Hz) activity across the lateral hemisphere in less than 1 sec. The sequence demonstrated concurrent regional sensory processing of speech syllables in the posterior superior temporal gyrus (STG) and speech motor cortex, and then transitioned to sequential task-dependent processing from prefrontal cortex (PFC), to the final motor response in the hand sensorimotor cortex. STG activation was modestly enhanced for target over nontarget sounds, supporting a selective gain mechanism in early sensory processing, whereas PFC was entirely selective to targets, supporting its role in guiding response behavior. These results reveal that target detection is not a single cognitive event, but rather a process of progressive target selectivity that involves large-scale rapid parallel and serial processing in sensory, cognitive, and motor structures to support goal-directed human behavior.

Comparison of time-frequency responses and the event related potential to auditory speech stimuli in the human cortex

Authors:

• Erik Edwards

• Maryam Soltani

• Won Kim

• Sarang S. Dalal

• Srikantan S. Nagarajan

• Mitchel S. Berger

• Robert T. Knight

Date: 2009

DOI: 10.1152/jn.90954.2008

PubMed: 19439673

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Abstract:

Comparison of time–frequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol 102: 377–386, 2009. First published May 13, 2009; doi:10.1152/jn.90954.2008. We recorded the electrocorticogram directly from the exposed cortical surface of awake neurosurgical patients during the presentation of auditory syllable stimuli. All patients were unanesthetized as part of a language-mapping procedure for subsequent left-hemisphere tumor resection. Time–frequency analyses showed significant high-gamma (
high : 70 –160 Hz) responses from the left superior temporal gyrus, but no reliable response from the left inferior frontal gyrus. Alpha suppression (: 7–14 Hz) and event-related potential responses exhibited a more widespread topography. Across electrodes, the  suppression from 200 to 450 ms correlated with the preceding (50 –200 ms)
high increase. The results are discussed in terms of the different physiological origins of these electrocortical signals.

Localization of neurosurgically implanted electrodes via photograph–MRI–radiograph coregistration

Authors:

• Sarang S. Dalal

• Erik Edwards

• Heidi E. Kirsch

• Nicholas M. Barbaro

• Robert T. Knight

• Srikantan S. Nagarajan

Date: 2008

DOI: 10.1016/j.jneumeth.2008.06.028

PubMed: 18657573

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Abstract:

Intracranial electroencephalography (iEEG) is clinically indicated for medically refractory epilepsy and is a promising approach for developing neural prosthetics. These recordings also provide valuable data for cognitive neuroscience research. Accurate localization of iEEG electrodes is essential for evaluating specific brain regions underlying the electrodes that indicate normal or pathological activity, as well as for relating research findings to neuroimaging and lesion studies. However, electrodes are frequently tucked underneath the edge of a craniotomy, inserted via a burr hole, or placed deep within the brain, where their locations cannot be verified visually or with neuronavigational systems. We show that one existing method, registration of postimplant computed tomography (CT) with preoperative magnetic resonance imaging (MRI), can result in errors exceeding 1 cm. We present a novel method for localizing iEEG electrodes using routinely acquired surgical photographs, X-ray radiographs, and magnetic resonance imaging scans. Known control points are used to compute projective transforms that link the different image sets, ultimately allowing hidden electrodes to be localized, in addition to refining the location of manually registered visible electrodes. As the technique does not require any calibration between the different image modalities, it can be applied to existing image databases. The final result is a set of electrode positions on the patient’s rendered MRI yielding locations relative to sulcal and gyral landmarks on individual anatomy, as well as MNI coordinates. We demonstrate the results of our method in eight epilepsy patients implanted with electrode grids spanning the left hemisphere.

Five-dimensional neuroimaging: localization of the time-frequency dynamics of cortical activity

Authors:

• Sarang S. Dalal

• Adrian G. Guggisberg

• Erik Edwards

• Kensuke Sekihara

• Anne M. Findlay

• Ryan T. Canolty

• Mitchel S. Berger

• Robert T. Knight

• Nicholas M. Barbaro

• Heidi E. Kirsch

• Srikantan S. Nagarajan

Date: 2008

DOI: 10.1016/j.neuroimage.2008.01.023

PubMed: 18356081

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Abstract:

The spatiotemporal dynamics of cortical oscillations across human brain regions remain poorly understood because of a lack of adequately validated methods for reconstructing such activity from noninvasive electrophysiological data. In this paper, we present a novel adaptive spatial filtering algorithm optimized for robust source time– frequency reconstruction from magnetoencephalography (MEG) and electroencephalography (EEG) data. The efficacy of the method is demonstrated with simulated sources and is also applied to real MEG data from a self-paced finger movement task. The algorithm reliably reveals modulations both in the beta band (12–30 Hz) and high gamma band (65–90 Hz) in sensorimotor cortex. The performance is validated by both across-subjects statistical comparisons and by intracranial electrocorticography (ECoG) data from two epilepsy patients. Inter- estingly, we also reliably observed high frequency activity (30–300 Hz) in the cerebellum, although with variable locations and frequencies across subjects. The proposed algorithm is highly parallelizable and runs efficiently on modern high-performance computing clusters. This method enables the ultimate promise of MEG and EEG for five- dimensional imaging of space, time, and frequency activity in the brain and renders it applicable for widespread studies of human cortical dynamics during cognition.

Spatiotemporal dynamics of word processing in the human brain

Authors:

• Ryan T. Canolty

• Maryam Soltani

• Sarang S. Dalal

• Erik Edwards

• Nina F. Dronkers

• Srikantan S. Nagarajan

• Heidi E. Kirsch

• Nicholas M. Barbaro

• Robert T. Knight

Date: 2007

PubMed: 18982128

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Abstract:

We examined the spatiotemporal dynamics of word processing by recording the electrocorticogram (ECoG) from the lateral frontotemporal cortex of neurosurgical patients chronically implanted with subdural electrode grids. Subjects engaged in a target detection task where proper names served as infrequent targets embedded in a stream of task-irrelevant verbs and nonwords. Verbs described actions related to the hand (e.g, throw) or mouth (e.g., blow), while unintelligible nonwords were sounds which matched the verbs in duration, intensity, temporal modulation, and power spectrum. Complex oscillatory dynamics were observed in the delta, theta, alpha, beta, low, and high gamma (HG) bands in response to presentation of all stimulus types. HG activity (80-200 Hz) in the ECoG tracked the spatiotemporal dynamics of word processing and identified a network of cortical structures involved in early word processing. HG was used to determine the relative onset, peak, and offset times of local cortical activation during word processing. Listening to verbs compared to nonwords sequentially activates first the posterior superior temporal gyrus (post-STG), then the middle superior temporal gyrus (mid-STG), followed by the superior temporal sulcus (STS). We also observed strong phase-locking between pairs of electrodes in the theta band, with weaker phase-locking occurring in the delta, alpha, and beta frequency ranges. These results provide details on the first few hundred milliseconds of the spatiotemporal evolution of cortical activity during word processing and provide evidence consistent with the hypothesis that an oscillatory hierarchy coordinates the flow of information between distinct cortical regions during goal-directed behavior.

Spatial localization of cortical time-frequency dynamics

Authors:

• Sarang S. Dalal

• Adrian G. Guggisberg

• Erik Edwards

• Kensuke Sekihara

• Anne M. Findlay

• Ryan T. Canolty

• Robert T. Knight

• Nicholas M. Barbaro

• Heidi E. Kirsch

• Srikantan S. Nagarajan

Date: 2007

PubMed: 18003115

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Abstract:

The spatiotemporal dynamics of cortical oscillations across human brain regions remain poorly understood because of a lack of adequately validated methods for reconstructing such activity from noninvasive electrophysiological data. We present a novel adaptive spatial filtering algorithm optimized for robust source time-frequency reconstruction from magnetoencephalography (MEG) and electroencephalography (EEG) data. The efficacy of the method is demonstrated with real MEG data from a self-paced finger movement task. The algorithm reliably reveals modulations both in the beta band (12-30 Hz) and a high gamma band (65-90 Hz) in sensorimotor cortex. The performance is validated by both across-subjects statistical comparisons and by intracranial electrocorticography (ECoG) data from two epilepsy patients. We also revealed observed high gamma activity in the cerebellum. The proposed algorithm is highly parallelizable and runs efficiently on modern high performance computing clusters. This method enables non-invasive five-dimensional imaging of space, time, and frequency activity in the brain and renders it applicable for widespread studies of human cortical dynamics.

High Gamma Power is Phase-Locked to Theta Oscillations in Human Neocortex

Authors:

• Ryan T. Canolty

• Erik Edwards

• Sarang S. Dalal

• Maryam Soltani

• Srikantan S. Nagarajan

• Heidi E. Kirsch

• Mitchel S. Berger

• Nicholas M. Barbaro

• Robert T. Knight

Date: 2006

PubMed: 16973878

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Abstract:

We observed robust coupling between the high- and low-frequency bands of ongoing electrical activity in the human brain. In particular, the phase of the low-frequency theta (4 to 8 hertz) rhythm modulates power in the high gamma (80 to 150 hertz) band of the electrocorticogram, with stronger modulation occurring at higher theta amplitudes. Furthermore, different behavioral tasks evoke distinct patterns of theta/high gamma coupling across the cortex. The results indicate that transient coupling between low- and high-frequency brain rhythms coordinates activity in distributed cortical areas, providing a mechanism for effective communication during cognitive processing in humans.

High gamma activity in response to deviant auditory stimuli recorded directly from human cortex

Authors:

• Erik Edwards

• Maryam Soltani

• Leon Y. Deouell

• Mitchel S. Berger

• Robert T. Knight

Date: 2005

PubMed: 16093343

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Abstract:

We recorded electrophysiological responses from the left frontal and temporal cortex of awake neurosurgical patients to both repetitive background and rare deviant auditory stimuli. Prominent sensory event-related potentials (ERPs) were recorded from auditory association cortex of the temporal lobe and adjacent regions surrounding the posterior Sylvian fissure. Deviant stimuli generated an additional longer latency mismatch response, maximal at more anterior temporal lobe sites. We found low gamma (30-60 Hz) in auditory association cortex, and we also show the existence of high-frequency oscillations above the traditional gamma range (high gamma, 60-250 Hz). Sensory and mismatch potentials were not reliably observed at frontal recording sites. We suggest that the high gamma oscillations are sensory-induced neocortical ripples, similar in physiological origin to the well-studied ripples of the hippocampus.

Synchronization measures of bursting data: Application to the electrocoricogram of an auditory event-related experiment

Authors:

• Mark A. Kramer

• Erik Edwards

• Maryam Soltani

• Mitchel S. Berger

• Robert T. Knight

• Andrew J. Szeri

Date: 2004

PubMed: 15324095

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Abstract:

Synchronization measures have become an important tool for exploring the relationships between time series. We review three recently proposed nonlinear synchronization measures and expand their definitions in a straightforward way to apply to an ensemble of measurements. We also develop a synchronization measure in which nearest neighbors are determined across the ensemble. We compare these four nonlinear synchronization measures and show that our measure succeeds in physically motivated examples where the other methods fail. We apply the synchronization measure to human electrocorticogram data collected during an auditory event-related potential experiment. The results suggest a crude model of cortical connectivity.