Temporal dynamics and response modulation across the human visual system in a spatial attention task: an ECoG study

Abstract:

The selection of behaviorally relevant information from cluttered visual scenes (often referred to as “attention”) is mediated by a cortical large-scale network consisting of areas in occipital, temporal, parietal, and frontal cortex that is organized into a functional hierarchy of feedforward and feedback pathways. In the human brain, little is known about the temporal dynamics of attentional processing from studies at the mesoscopic level of electrocorticography (ECoG), that combines millisecond temporal resolution with precise anatomical localization of recording sites. We analyzed high-frequency broadband responses (HFB) responses from 626 electrodes implanted in 8 epilepsy patients who performed a spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system. HFB responses showed high spatial selectivity and tuning, constituting ECoG response fields (RFs), within and outside the topographic visual system. In accordance with monkey physiology studies, both RF widths and onset latencies increased systematically across the visual processing hierarchy. We used the spatial specificity of HFB responses to quantitatively study spatial attention effects and their temporal dynamics to probe a hierarchical top-down model suggesting that feedback signals back propagate the visual processing hierarchy. Consistent with such a model, the strengths of attentional modulation were found to be greater and modulation latencies to be shorter in posterior parietal cortex, middle temporal cortex and ventral extrastriate cortex compared with early visual cortex. However, inconsistent with such a model, attention effects were weaker and more delayed in anterior parietal and frontal cortex.

Authors:

• Anne B. Martin

• Xiaofang Yang

• Yuri B. Saalmann

• Liang Wang

• Avgusta Shestyuk

• Jack J. Lin

• Josef Parvizi

• Robert T. Knight

• Sabine Kastner

Date: 2019

DOI: 10.1523/JNEUROSCI.1889-18.2018

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Encoding of multiple reward-related computations in transient and sustained high-frequency activity in human OFC

Abstract:

Human orbitofrontal cortex (OFC) has long been implicated in value-based decision making. In recent years, convergent evidence from human and model organisms has further elucidated its role in representing reward-related computations underlying decision making. However, a detailed description of these processes remains elusive due in part to (1) limitations in our ability to observe human OFC neural dynamics at the timescale of decision processes and (2) methodological and interspecies differences that make it challenging to connect human and animal findings or to resolve discrepancies when they arise. Here, we sought to address these challenges by conducting multi-electrode electrocorticography(ECoG) recordings in neurosurgical patients during economic decision making to elucidate the electrophysiological signature, sub-second temporal profile, and anatomical distribution of reward-related computations within human OFC. We found that high-frequency activity (HFA) (70–200 Hz) reflected multiple valuation components grouped in two classes of valuation signals that were dissociable in temporal profile and information content: (1) fast, transient responses reflecting signals associated with choice and outcome processing, including anticipated risk and outcome regret, and (2) sustained responses explicitly encoding what happened in the immediately preceding trial. Anatomically, these responses were widely distributed in partially overlapping networks, including regions in the central OFC (Brodmann areas 11 and 13), which have been consistently implicated in reward processing in animal single-unit studies. Together, these results integrate insights drawn from human and animal studies and provide evidence for a role of human OFC in representing multiple reward computations.

Authors:

• Ignacio Saez

• Jack Lin

• Arjen Stolk

• Edward Chang

• Josef Parvizi

• Gerwin Schalk

• Robert T. Knight

• Ming Hsu

Date: 2018

DOI: 10.1016/j.cub.2018.07.045

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Neural mechanisms of sustained attention are rhythmic

ABSTRACT

Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.

AUTHORS

• Randolph F. Helfrich

• Ian C. Fiebelkorn

• Sara M. Szczepanski

• Jack J. Lin

• Josef Parvizi

• Robert T. Knight

• Sabine Kastner

Date: 2018

DOI: 10.1016/j.neuron.2018.07.032

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Persistent neuronal activity in human prefrontal cortex links perception and action

ABSTRACT

How do humans flexibly respond to changing environmental demands on a subsecond temporal scale? Extensive research has highlighted the key role of the prefrontal cortex in flexible decision-making and adaptive behaviour, yet the core mechanisms that translate sensory information into behaviour remain undefined. Using direct human cortical recordings, we investigated the temporal and spatial evolution of neuronal activity (indexed by the broadband gamma signal) in 16 participants while they performed a broad range of self-paced cognitive tasks. Here we describe a robust domain- and modality-independent pattern of persistent stimulus-to-response neural activation that encodes stimulus features and predicts motor output on a trial-by-trial basis with near-perfect accuracy. Observed across a distributed network of brain areas, this persistent neural activation is centred in the prefrontal cortex and is required for successful response implementation, providing a functional substrate for domain-general transformation of perception into action, critical for flexible behaviour.

AUTHORS

• Matar Haller

• John Case

• Nathan E. Crone

• Edward F. Chang

• David King-Stephens

• Kenneth D. Laxer

• Peter B. Weber

• Josef Parvizi

• Robert T. Knight

• Avgusta Y. Shestyuk

Date: 2017

DOI: 10.1038/s41562-017-0267-2

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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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Mirroring in the Human Brain: Deciphering the Spatial-Temporal Patterns of the Human Mirror Neuron System

ABSTRACT

Embodied theories of cognition emphasize the central role of sensorimotor transformations in the representation of others’ actions. Support for these theories is derived from the discovery of the mirror neuron system (MNS) in primates, from noninvasive techniques in humans, and from a limited number of intracranial studies. To understand the neural dynamics of the human MNS, more studies with precise spatial and temporal resolutions are essential. We used electrocorticography to define activation patterns in sensorimotor, parietal and/or frontal neuronal populations, during a viewing and grasping task. Our results show robust high gamma activation for both conditions in classic MNS sites. Furthermore, we provide novel evidence for 2 different populations of neurons: sites that were only active for viewing and grasping (“pure mirroring”) and sites that were also active between viewing and grasping, and perhaps serve a more general attentional role. Lastly, a subgroup of parietal electrodes showed earlier peaks than all other regions. These results highlight the complexity of spatial-temporal patterns within the MNS and provide a critical link between single-unit research in monkeys and noninvasive techniques in human.

AUTHORS

• Anat Perry

• Jennifer Stiso

• Edward F Chang

• Jack J Lin

• Josef Parvizi

• Robert T Knight

Date: 2017

DOI: 10.1093/cercor/bhx013

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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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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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Frontal and motor cortex contributions to response inhibition: evidence from electrocorticography

ABSTRACT

Changes in the environment require rapid modification or inhibition of ongoing behavior. We used the stop-signal paradigm and intracranial recordings to investigate response preparation, inhibition, and monitoring of task-relevant information. Electrocorticographic data were recorded in eight patients with electrodes covering frontal, temporal, and parietal cortex, and time-frequency analysis was used to examine power differences in the beta (13–30 Hz) and high-gamma bands (60 –180 Hz). Over motor cortex, beta power decreased, and high-gamma power increased during motor preparation for both go trials (Go) and unsuccessful stops (US). For successful stops (SS), beta increased, and high-gamma was reduced, indexing the cancellation of the prepared response. In the middle frontal gyrus (MFG), stop signals elicited a transient high-gamma increase. The MFG response occurred before the estimated stop-signal reaction time but did not distinguish between SS and US trials, likely signaling attention to the salient stop stimulus. A postresponse high-gamma increase in MFG was stronger for US compared with SS and absent in Go, supporting a role in behavior monitoring. These results provide evidence for differential contributions of frontal subregions to response inhibition, including motor preparation and inhibitory control in motor cortex and cognitive control and action evaluation in lateral prefrontal cortex.

AUTHORS

• Y.M. Fonken

• Jochem W. Rieger

• Elinor Tzvi

• Nathan E. Crone

• Edward F. Chang

• Josef Parvizi

• Robert T. Knight

• Ulrike M. Krämer

Date: 2016

DOI: 10.1038/srep25803

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Amygdala and Orbitofrontal engagement in breach and resolution of expectancy - a case study

ABSTRACT

Humans constantly predict their environment to facilitate mutual interaction. Predictions are connected with emotions as nonfatal penalties and rewards (for incorrect and correct expectancies, respectively) that result in negative and positive emotions. Music is an ideal stimulus to explore the underlying neurophysiological mechanisms of prediction related emotions. Using the high spatial and temporal resolution of stereotactic depth electrodes, we identified activation patterns and examined their distribution in the bilateral Amygdalae and the orbitofrontal cortex (OFC). We used music excerpts with either (a) a deceptive cadence (i.e., an unexpected chord/breach) or (b) a tonic chord inserted instead of a deceptive cadence (regular chord/no breach). These events were followed by a chord progression leading to and ending on the tonic after a breach (c) or (d) on a tonic after no breach. We computed the differences of the analytic amplitudes in the theta band at these time-points (i.e., events a–d) by using t tests. We found a significant difference between the unexpected chord (a) and the expected chord (b) in the analytic amplitude of the theta band in the left amygdala. Further we found a difference between the 2 resolutions (c and d) in the analytic amplitude of the theta band within the OFC. In conclusion, our case study supports the notion that the amygdala and the OFC are important for emotional responses to musical expectancy breaches as well as of their resolution. (PsycINFO Database Record (c) 2016 APA, all rights reserved)

AUTHORS

• Christian Mikutta

• S. Durschmid

• Nelson Bean

• Moritz Lehne

• James Lubell

• Andreas Altorfer

• Josef Parvizi

• Werner K. Strik

• Robert T. Knight

• Stefan Koelsch

Date: 2015

DOI: dx.doi.org/10.1037/pmu0000121

Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

Abstract:

Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4–8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80–150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

Authors:

• Bradley Voytek

• Andrew S. Kayser

• David Badre

• David Fegen

• Edward F. Chang

• Nathan E. Crone

• Josef Parvizi

• Robert T. Knight

• Mark D'Esposito

Date: 2015

DOI: 10.1038/nn.4071

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Dynamic changes in phase-amplitude coupling facilitate spatial attention control in fronto-parietal cortex

Authors:

• Sara Szczepanski

• Nathan E. Crone

• Rachel A. Kuperman

• Kurtis I. Auguste

• Josef Parvizi

• Robert T. Knight

Date: 2014

DOI: 10.1371/journal.pbio.1001936

PubMed: 4144794

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Abstract:

Attention is a core cognitive mechanism that allows the brain to allocate limited resources depending on current task demands. A number of frontal and posterior parietal cortical areas, referred to collectively as the fronto-parietal attentional control network, are engaged during attentional allocation in both humans and non-human primates. Numerous studies have examined this network in the human brain using various neuroimaging and scalp electrophysiological techniques. However, little is known about how these frontal and parietal areas interact dynamically to produce behavior on a fine temporal (sub-second) and spatial (sub-centimeter) scale. We addressed how human fronto-parietal regions control visuospatial attention on a fine spatiotemporal scale by recording electrocorticography (ECoG) signals measured directly from subdural electrode arrays that were implanted in patients undergoing intracranial monitoring for localization of epileptic foci. Subjects (n=8) performed a spatial-cuing task, in which they allocated visuospatial attention to either the right or left visual field and detected the appearance of a target. We found increases in high gamma (HG) power (70–250 Hz) time-locked to trial onset that remained elevated throughout the attentional allocation period over frontal, parietal, and visual areas. These HG power increases were modulated by the phase of the ongoing delta/theta (2–5 Hz) oscillation during attentional allocation. Critically, we found that the strength of this delta/theta phase-HG amplitude coupling predicted reaction times to detected targets on a trial-by-trial basis. These results highlight the role of delta/theta phase-HG amplitude coupling as a mechanism for sub-second facilitation and coordination within human fronto-parietal cortex that is guided by momentary attentional demands.

Proceedings of the Third International Workshop on Advances in Electrocorticography

Authors:

• Anthony Ritaccio

• Michael Beauchamp

• Conrado Bosman

• Peter Brunner

• Edward F. Chang

• Nathan E. Crone

• Ayesegul Gunduz

• Disha Gupta

• Robert T. Knight

• Eric Leuthardt

• Brian Litt

• Daniel Moran

• Jeffrey G. Ojemann

• Josef Parvizi

• Nick F. Ramsey

• Jochem W. Rieger

• Jonathan Viventi

• Bradley Voytek

• Justin Williams

• Gerwin Schalk

Date: 2012

DOI: 10.1016/j.yebeh.2012.09.016

PubMed: 23160096

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Abstract:

The Third International Workshop on Advances in Electrocorticography (ECoG) was convened in Washington, DC, on November 10–11, 2011. As in prior meetings, a true multidisciplinary fusion of clinicians, scientists, and engineers from many disciplines gathered to summarize contemporary experiences in brain surface recordings. The proceedings of this meeting serve as evidence of a very robust and transformative field but will yet again require revision to incorporate the advances that the following year will surely bring.

Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks

Authors:

• Bradley Voytek

• Ryan T. Canolty

• Avgusta Shestyuk

• Nathan E. Crone

• Josef Parvizi

• Robert T. Knight

Date: 2010

DOI: 10.3389/fnhum.2010.00191

PubMed: 21060716

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Abstract:

The phase of ongoing theta (4–8 Hz) and alpha (8–12 Hz) electrophysiological oscillations is coupled to high gamma (80–150 Hz) amplitude, which suggests that low-frequency oscillations modulate local cortical activity. While this phase–amplitude coupling (PAC) has been demonstrated in a variety of tasks and cortical regions, it has not been shown whether task demands differentially affect the regional distribution of the preferred low-frequency coupling to high gamma. To address this issue we investigated multiple-rhythm theta/alpha to high gamma PAC in two subjects with implanted subdural electrocorticographic grids. We show that high gamma amplitude couples to the theta and alpha troughs and demonstrate that, during visual tasks, alpha/high gamma coupling preferentially increases in visual cortical regions. These results suggest that low-frequency phase to high-frequency amplitude coupling is modulated by behavioral task and may reflect a mechanism for selection between communicating neuronal networks.