Intracranial recordings demonstrate medial temporal lobe engagement in visual search in humans

Abstract:

Visual search is a fundamental human behavior, which has been proposed to include two component processes: inefficient search (Search) and efficient search (Pop-out). According to extant research, these two processes map onto two separable neural systems located in the frontal and parietal association cortices. In the present study, we use intracranial recordings from 23 participants to delineate the neural correlates of Search and Pop-out with an unprecedented combination of spatiotemporal resolution and coverage across cortical and subcortical structures. First, we demonstrate a role for the medial temporal lobe in visual search, on par with engagement in frontal and parietal association cortex. Second, we show a gradient of increasing engagement over anatomical space from dorsal to ventral lateral frontal cortex. Third, we confirm previous work demonstrating nearly complete overlap in neural engagement across cortical regions in Search and Pop-out. We further demonstrate Pop-out selectivity manifesting as activity increase in Pop-out as compared to Search in a distributed set of sites including frontal cortex. This result is at odds with the view that Pop-out is implemented in low-level visual cortex or parietal cortex alone. Finally, we affirm a central role for the right lateral frontal cortex in Search.

Authors:

• S. J. Katarina Slama

• Richard Jimenez

• Sujayam Saha

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Tor Endestad

• Pål G Larsson

• Anne-Kristin Solbakk

• Jack J Lin

• Robert T Knight

Date: 2021

DOI: https://doi.org/10.1162/jocn_a_01739

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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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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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Auditory deviance detection in the human insula: An intracranial EEG study

Abstract:

The human insula is known to be involved in auditory processing, but knowledge about its precise functional role and the underlying electrophysiology is limited. To assess its role in automatic auditory deviance detection we analyzed the EEG high frequency activity (HFA; 75–145 Hz) and ERPs from 90 intracranial insular channels across 16 patients undergoing pre-surgical intracranial monitoring for epilepsy treatment. Subjects passively listened to a stream of standard and deviant tones differing in four physical dimensions: intensity, frequency, location or time. HFA responses to auditory stimuli were found in the short and long gyri, and the anterior, superior, and inferior segments of the circular sulcus of the insular cortex. Only a subset of channels in the inferior segment of the circular sulcus of the insula showed HFA deviance detection responses, i.e., a greater and longer latency response to specific deviants relative to standards. Auditory deviancy processing was also later in the insula when compared with the superior temporal cortex. ERP results were more widespread and supported the HFA insular findings. These results provide evidence that the human insula is engaged during auditory deviance detection.

Authors:

• Alejandro O Blenkmann

• Santiago Collavini

• James Lubell

• Anaïs Llorens

• Ingrid Funderud

• Jugoslav Ivanovic

• Pål G Larsson

• Torstein R Meling

• Tristan Bekinschtein

• Silvia Kochen

• Tor Endestad

• Robert T Knight

• Anne-Kristin Solbakk

Date: 2019

DOI: https://doi.org/10.1016/j.cortex.2019.09.002

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