Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study

Abstract:

Context modulates sensory neural activations enhancing perceptual and behavioral performance and reducing prediction errors. However, the mechanism of when and where these high-level expectations act on sensory processing is unclear. Here, we isolate the effect of expectation absent of any auditory evoked activity by assessing the response to omitted expected sounds. Electrocorticographic signals were recorded directly from subdural electrode grids placed over the superior temporal gyrus (STG). Subjects listened to a predictable sequence of syllables, with some infrequently omitted. We found high-frequency band activity (HFA, 70–170 Hz) in response to omissions, which overlapped with a posterior subset of auditory-active electrodes in STG. Heard syllables could be distinguishable reliably from STG, but not the identity of the omitted stimulus. Both omission- and target-detection responses were also observed in the prefrontal cortex. We propose that the posterior STG is central for implementing predictions in the auditory environment. HFA omission responses in this region appear to index mismatch-signaling or salience detection processes.

Authors:

• Hohyun Cho

• Yvonne M Fonken

• Markus Adamek

• Richard Jimenez

• Jack J Lin

• Gerwin Schalk

• Robert T Knight

• Peter Brunner

Date: 2023

DOI: https://doi.org/10.1093/cercor/bhad155

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Gender bias in academia: A lifetime problem that needs solutions

Summary:

Despite increased awareness of the lack of gender equity in academia and a growing number of initiatives to address issues of diversity, change is slow, and inequalities remain. A major source of inequity is gender bias, which has a substantial negative impact on the careers, work-life balance, and mental health of underrepresented groups in science. Here, we argue that gender bias is not a single problem but manifests as a collection of distinct issues that impact researchers’ lives. We disentangle these facets and propose concrete solutions that can be adopted by individuals, academic institutions, and society.

Authors:

• Anaïs Llorens

• Athina Tzovara

• Ludovic Bellier

• Ilina Bhaya-Grossman

• Aurélie Bidet-Caulet

• William K Chang

• Zachariah R Cross

• Rosa Dominguez-Faus

• Adeen Flinker

• Yvonne Fonken

• Mark A Gorenstein

• Chris Holdgraf

• Colin W Hoy

• Maria V Ivanova

• Richard T Jimenez

• Soyeon Jun

• Julia WY Kam

• Celeste Kidd

• Enitan Marcelle

• Deborah Marciano

• Stephanie Martin

• Nicholas E Myers

• Karita Ojala

• Anat Perry

• Pedro Pinheiro-Chagas

• Stephanie K Riès

• Ignacio Saez

• Ivan Skelin

• Katarina Slama

• Brooke Staveland

• Danielle S Bassett

• Elizabeth A Buffalo

• Adrienne L Fairhall

• Nancy J Kopell

• Laura J Kray

• Jack J Lin

• Anna C Nobre

• Dylan Riley

• Anne-Kristin Solbakk

• Joni D Wallis

• Xiao-Jing Wang

• Shlomit Yuval-Greenberg

• Sabine Kastner

• Robert T Knight

• Nina F Dronkers

Date: 2021

DOI: https://doi.org/10.1016/j.neuron.2021.06.002

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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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An electrophysiological marker of arousal level in humans

Abstract:

Deep non-rapid eye movement sleep (NREM) and general anesthesia with propofol are prominent states of reduced arousal linked to the occurrence of synchronized oscillations in the electroencephalogram (EEG). Although rapid eye movement (REM) sleep is also associated with diminished arousal levels, it is characterized by a desynchronized, ‘wake-like’ EEG. This observation implies that reduced arousal states are not necessarily only defined by synchronous oscillatory activity. Using intracranial and surface EEG recordings in four independent data sets, we demonstrate that the 1/f spectral slope of the electrophysiological power spectrum, which reflects the non-oscillatory, scale-free component of neural activity, delineates wakefulness from propofol anesthesia, NREM and REM sleep. Critically, the spectral slope discriminates wakefulness from REM sleep solely based on the neurophysiological brain state. Taken together, our findings describe a common electrophysiological marker that tracks states of reduced arousal, including different sleep stages as well as anesthesia in humans.

Authors:

• Janna D Lendner

• Randolph F Helfrich

• Bryce A Mander

• Luis Romundstad

• Jack J Lin

• Matthew P Walker

• Pal G Larsson

• Robert T Knight

Date: 2020

DOI: https://doi.org/10.7554/eLife.55092

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Coupling between slow-waves and sharp-wave ripples organizes distributed neural activity during sleep in humans

Abstract:

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80-150 Hz) and subcortical/cortical slow-waves (0.5-4 Hz). However, the precise role of SWR-slow-wave interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, temporal and frontal cortices, to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high frequency activity (HFA; 70-200 Hz) a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical slow-waves. Finally, local cortical slow-wave phase offsets during SWRs predicted functional connectivity between the frontal and temporal cortex. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

Authors:

• Ivan Skelin

• Haoxin Zhang

• Jie Zheng

• Shiting Ma

• Bryce A Mander

• Olivia Kim Mcmanus

• Sumeet Vadera

• Robert T Knight

• Bruce L McNaughton

• Jack J Lin

Date: 2020

DOI: https://doi.org/10.1101/2020.05.24.113480

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Default network and frontoparietal control network theta connectivity supports internal attention

Abstract:

Attending to our inner world is a fundamental cognitive phenomenon, yet its neural underpinnings remain largely unknown. Neuroimaging evidence implicates the default network (DN) and frontoparietal control network (FPCN); however, the electrophysiological basis for the interaction between these networks is unclear. Here we recorded intracranial electroencephalogram from DN and FPCN electrodes implanted in individuals undergoing presurgical monitoring for refractory epilepsy. Subjects performed an attention task during which they attended to tones (that is, externally directed attention) or ignored the tones and thought about whatever came to mind (that is, internally directed attention). Given the emerging role of theta band connectivity in attentional processes, we examined the theta power correlation between DN and two subsystems of the FPCN as a function of attention states. We found increased connectivity between DN and FPCNA during internally directed attention compared to externally directed attention, which positively correlated with attention ratings. There was no statistically significant difference between attention states in the connectivity between DN and FPCNB. Our results indicate that enhanced theta band connectivity between the DN and FPCNA is a core electrophysiological mechanism that underlies internally directed attention.

Authors:

• Julia WY Kam

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G Larsson

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41562-019-0717-0

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Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Abstract:

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Authors:

• Randolph F Helfrich

• Janna D Lendner

• Bryce A Mander

• Heriberto Guillen

• Michelle Paff

• Lilit Mnatsakanyan

• Sumeet Vadera

• Matthew P Walker

• Jack J Lin

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-11444-x

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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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