A rapid theta network mechanism for flexible information encoding

Abstract:

Flexible behavior requires gating mechanisms that encode only task-relevant information in working memory. Extant literature supports a theoretical division of labor whereby lateral frontoparietal interactions underlie information maintenance and the striatum enacts the gate. Here, we reveal neocortical gating mechanisms in intracranial EEG patients by identifying rapid, within-trial changes in regional and inter-regional activities that predict subsequent behavioral outputs. Results first demonstrate information accumulation mechanisms that extend prior fMRI (i.e., regional high-frequency activity) and EEG evidence (inter-regional theta synchrony) of distributed neocortical networks in working memory. Second, results demonstrate that rapid changes in theta synchrony, reflected in changing patterns of default mode network connectivity, support filtering. Graph theoretical analyses further linked filtering in task-relevant information and filtering out irrelevant information to dorsal and ventral attention networks, respectively. Results establish a rapid neocortical theta network mechanism for flexible information encoding, a role previously attributed to the striatum.

Authors:

• Elizabeth L. Johnson

• Jack J. Lin

• David King-Stephens

• Peter B. Weber

• Kenneth D. Laxer

• Ignacio Saez

• Fady Girgis

• Mark D’Esposito

• Robert T. Knight

• David Badre

Date: 2023

DOI: https://doi.org/10.1038/s41467-023-38574-7

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Orbitofrontal cortex governs working memory for temporal order

Abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory1, which may contribute to confabulation in individuals with OFC damage2. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage2 may relate to impaired temporal-order understanding.

Authors:

• Elizabeth L. Johnson

• William K. Chang

• Callum D. Dewar

• Donna Sorensen

• Jack J. Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Donatella Scabini

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.cub.2022.03.074

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Prefrontal Lesions Disrupt Posterior Alpha–Gamma Coordination of Visual Working Memory Representations

Abstract:

How does the human brain prioritize different visual representations in working memory (WM)? Here, we define the oscillatory mechanisms supporting selection of “where” and “when” features from visual WM storage and investigate the role of pFC in feature selection. Fourteen individuals with lateral pFC damage and 20 healthy controls performed a visuospatial WM task while EEG was recorded. On each trial, two shapes were presented sequentially in a top/bottom spatial orientation. A retro-cue presented mid-delay prompted which of the two shapes had been in either the top/bottom spatial position or first/second temporal position. We found that cross-frequency coupling between parieto-occipital alpha (α; 8–12 Hz) oscillations and topographically distributed gamma (γ; 30–50 Hz) activity tracked selection of the distinct cued feature in controls. This signature of feature selection was disrupted in patients with pFC lesions, despite intact α–γ coupling independent of feature selection. These findings reveal a pFC-dependent parieto-occipital α–γ mechanism for the rapid selection of visual WM representations.

Authors:

• Saeideh Davoudi

• Mohsen Parto Dezfouli

• Robert T. Knight

• Mohammad Reza Daliri

• Elizabeth L. Johnson

Date: 2021

DOI: https://doi.org/10.1162/jocn_a_01715

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Spectral imprints of working memory for everyday associations in the frontoparietal network

ABSTRACT

How does the human brain rapidly process incoming information in working memory? In growing divergence from a single-region focus on the prefrontal cortex (PFC), recent work argues for emphasis on how distributed neural networks are rapidly coordinated in support of this central neurocognitive function. Previously, we showed that working memory for everyday “what,” “where,” and “when” associations depends on multiplexed oscillatory systems, in which signals of different frequencies simultaneously link the PFC to parieto-occipital and medial temporal regions, pointing to a complex web of sub-second, bidirectional interactions. Here, we used direct brain recordings to delineate the frontoparietal oscillatory correlates of working memory with high spatiotemporal precision. Seven intracranial patients with electrodes simultaneously localized to prefrontal and parietal cortices performed a visuospatial working memory task that operationalizes the types of identity and spatiotemporal information we encounter every day. First, task-induced oscillations in the same delta-theta (2–7 Hz) and alpha-beta (9–24 Hz) frequency ranges previously identified using scalp electroencephalography (EEG) carried information about the contents of working memory. Second, maintenance was linked to directional connectivity from the parietal cortex to the PFC. However, presentation of the test prompt to cue identity, spatial, or temporal information changed delta-theta coordination from a unidirectional, parietal-led system to a bidirectional, frontoparietal system. Third, the processing of spatiotemporal information was more bidirectional in the delta-theta range than was the processing of identity information, where alpha-beta connectivity did not exhibit sensitivity to the contents of working memory. These findings implicate a bidirectional delta-theta mechanism for frontoparietal control over the contents of working memory.

AUTHORS

• Elizabeth L. Johnson

• David King-Stephens

• Peter B. Weber

• Kenneth D. Laxer

• Jack J. Lin

• Robert T. Knight

Date: 2019

DOI: 10.3389/fnsys.2018.00065

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Dynamic frontotemporal systems process space and time in working memory

ABSTRACT

How do we rapidly process incoming streams of information in working memory, a cognitive mechanism central to human behavior? Dominant views of working memory focus on the prefrontal cortex (PFC), but human hippocampal recordings provide a neurophysiological signature distinct from the PFC. Are these regions independent, or do they interact in the service of working memory? We addressed this core issue in behavior by recording directly from frontotemporal sites in humans performing a visuospatial working memory task that operationalizes the types of identity and spatiotemporal information we encounter every day. Theta band oscillations drove bidirectional interactions between the PFC and medial temporal lobe (MTL; including the hippocampus). MTL theta oscillations directed the PFC preferentially during the processing of spatiotemporal information, while PFC theta oscillations directed the MTL for all types of information being processed in working memory. These findings reveal an MTL theta mechanism for processing space and time and a domain-general PFC theta mechanism, providing evidence that rapid, dynamic MTL–PFC interactions underlie working memory for everyday experiences.

AUTHORS

• Elizabeth L. Johnson

• Jenna N. Adams

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Jack J. Lin

• Robert T. Knight

Date: 2018

DOI: 10.1371/journal.pbio.2004274

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Bidirectional frontoparietal oscillatory systems support working memory

ABSTRACT

The ability to represent and select information in working memory provides the neurobiological infrastructure for human cognition. For 80 years, dominant views of working memory have focused on the key role of prefrontal cortex (PFC). However, more recent work has implicated posterior cortical regions, suggesting that PFC engagement during working memory is dependent on the degree of executive demand. We provide evidence from neurological patients with discrete PFC damage that challenges the dominant models attributing working memory to PFC-dependent systems. We show that neural oscillations, which provide a mechanism for PFC to communicate with posterior cortical regions, independently subserve communications both to and from PFC—uncovering parallel oscillatory mechanisms for working memory. Fourteen PFC patients and 20 healthy, age-matched controls performed a working memory task where they encoded, maintained, and actively processed information about pairs of common shapes. In controls, the electroencephalogram (EEG) exhibited oscillatory activity in the low-theta range over PFC and directional connectivity from PFC to parieto-occipital regions commensurate with executive processing demands. Concurrent alpha-beta oscillations were observed over parieto-occipital regions, with directional connectivity from parieto-occipital regions to PFC, regardless of processing demands. Accuracy, PFC low-theta activity, and PFC / parieto-occipital connectivity were attenuated in patients, revealing a PFC-independent, alpha-beta system. The PFC patients still demonstrated task proficiency, which indicates that the posterior alpha-beta system provides sufficient resources for working memory. Taken together, our findings reveal neurologically dissociable PFC and parieto-occipital systems and suggest that parallel, bidirectional oscillatory systems form the basis of working memory.

AUTHORS

• Elizabeth L. Johnson

• Callum Dewar

• Anne-Kristin Solbakk

• Tor Endestad

• Torstein Meling

• Robert T. Knight

Date: 2017

DOI: 10.1016/j.cub.2017.05.046

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Intracranial recordings and human memory

Authors:

• Elizabeth L. Johnson

• Robert T. Knight

Date: 2015

DOI: 10.1016/j.conb.2014.07.021

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Abstract:

Recent work involving intracranial recording during human memory performance provides superb spatiotemporal resolution on mnemonic processes. These data demonstrate that the cortical regions identified in neuroimaging studies of memory fall into temporally distinct networks and the hippocampal theta activity reported in animal memory literature also plays a central role in human memory. Memory is linked to activity at multiple interacting frequencies, ranging from 1 to 500 Hz. High-frequency responses and coupling between different frequencies suggest that frontal cortex activity is critical to human memory processes, as well as a potential key role for the thalamus in neocortical oscillations. Future research will inform unresolved questions in the neuroscience of human memory and guide creation of stimulation protocols to facilitate function in the damaged brain.