Diverse Temporal Dynamics of Repetition Suppression Revealed by Intracranial Recordings in the Human Ventral Temporal Cortex

Abstract:

Repeated stimulus presentations commonly produce decreased neural responses—a phenomenon known as repetition suppression (RS) or adaptation—in ventral temporal cortex (VTC) of humans and nonhuman primates. However, the temporal features of RS in human VTC are not well understood. To fill this gap in knowledge, we utilized the precise spatial localization and high temporal resolution of electrocorticography (ECoG) from nine human subjects implanted with intracranial electrodes in the VTC. The subjects viewed nonrepeated and repeated images of faces with long-lagged intervals and many intervening stimuli between repeats. We report three main findings: 1) robust RS occurs in VTC for activity in high-frequency broadband (HFB), but not lower-frequency bands; 2) RS of the HFB signal is associated with lower peak magnitude (PM), lower total responses, and earlier peak responses; and 3) RS effects occur early within initial stages of stimulus processing and persist for the entire stimulus duration. We discuss these findings in the context of early and late components of visual perception, as well as theoretical models of repetition suppression.

Authors:

• Vinitha Rangarajan

• Corentin Jacques

• Robert T Knight

• Kevin S Weiner

• Kalanit Grill-Spector

Date: 2020

DOI: https://doi.org/10.1093/cercor/bhaa173

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Top–Down Attentional Modulation in Human Frontal Cortex: Differential Engagement during External and Internal Attention

Abstract:

Decades of electrophysiological research on top–down control converge on the role of the lateral frontal cortex in facilitating attention to behaviorally relevant external inputs. However, the involvement of frontal cortex in the top–down control of attention directed to the external versus internal environment remains poorly understood. To address this, we recorded intracranial electrocorticography while subjects directed their attention externally to tones and responded to infrequent target tones, or internally to their own thoughts while ignoring the tones. Our analyses focused on frontal and temporal cortices. We first computed the target effect, as indexed by the difference in high frequency activity (70–150 Hz) between target and standard tones. Importantly, we then compared the target effect between external and internal attention, reflecting a top–down attentional effect elicited by task demands, in each region of interest. Both frontal and temporal cortices showed target effects during external and internal attention, suggesting this effect is present irrespective of attention states. However, only the frontal cortex showed an enhanced target effect during external relative to internal attention. These findings provide electrophysiological evidence for top–down attentional modulation in the lateral frontal cortex, revealing preferential engagement with external attention.

Authors:

• Julia WY Kam

• Randolph F Helfrich

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G Larsson

• Jack J Lin

• Robert T Knight

Date: 2020

DOI: https://doi.org/10.1093/cercor/bhaa262

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Direct evidence for prediction signals in frontal cortex independent of prediction error

ABSTRACT

Predictive coding (PC) has been suggested as one of the main mechanisms used by brains to interact with complex environments. PC theories posit top-down prediction signals, which are compared with actual outcomes, yielding in turn prediction error (PE) signals, which are used, bottom-up, to modify the ensuing predictions. However, disentangling prediction from PE signals has been challenging. Critically, while many studies found indirect evidence for PC in the form of PE signals, direct evidence for the prediction signal is mostly lacking. Here, we provide clear evidence, obtained from intracranial cortical recordings in human surgical patients, that the human lateral prefrontal cortex evinces prediction signals while anticipating an event. Patients listened to task-irrelevant sequences of repetitive tones including infrequent predictable or unpredictable pitch deviants. The broadband high-frequency amplitude (HFA) was decreased prior to the onset of expected relative to unexpected deviants in the frontal cortex only, and its amplitude was sensitive to the increasing likelihood of deviants following longer trains of standards in the unpredictable condition. Single-trial HFA predicted deviations and correlated with poststimulus response to deviations. These results provide direct evidence for frontal cortex prediction signals independent of PE signals.

AUTHORS

• Stefan Dürschmid

• Christoph Reichert

• Hermann Hinrichs

• Hans-Jochen Heinze

• Heidi E Kirsch

• Robert T Knight

• Leon Y Deouell

Date: 2018

DOI: 10.1093/cercor/bhy331

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Lesions to the fronto-parietal network impact alpha-band phase synchrony and cognitive control

Abstract:

Long-range phase synchrony in the α-oscillation band (near 10 Hz) has been proposed to facilitate information integration across anatomically segregated regions. Which areas may top-down regulate such cross-regional integration is largely unknown. We previously found that the moment-to-moment strength of high-α band (10–12 Hz) phase synchrony co-varies with activity in a fronto-parietal (FP) network. This network is critical for adaptive cognitive control functions such as cognitive flexibility required during set-shifting. Using electroencephalography (EEG) in 23 patients with focal frontal lobe lesions (resected tumors), we tested the hypothesis that the FP network is necessary for modulation of high-α band phase synchrony. Global phase-synchrony was measured using an adaptation of the phase-locking value (PLV) in a sliding window procedure, which allowed for measurement of changes in EEG-based resting-state functional connectivity across time. As hypothesized, the temporal modulation (range and standard deviation) of high-α phase synchrony was reduced as a function of FP network lesion extent, mostly due to dorsolateral prefrontal cortex (dlPFC) lesions. Furthermore, patients with dlPFC lesions exhibited reduced cognitive flexibility as measured by the Trail-Making Test (set-shifting). Our findings provide evidence that the FP network is necessary for modulatory control of high-α band long-range phase synchrony, and linked to cognitive flexibility.

Authors:

• Sepideh Sadaghiani

• Pascasie L Dombert

• Marianne Løvstad

• Ingrid Funderud

• Torstein R Meling

• Tor Endestad

• Robert T Knight

• Anne-Kristin Solbakk

• Mark D’Esposito

Date: 2018

DOI: 10.1093/cercor/bhy296

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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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