Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex

Abstract:

The signed value and unsigned salience of reward prediction errors (RPEs) are critical to understanding reinforcement learning (RL) and cognitive control. Dorsomedial prefrontal cortex (dMPFC) and insula (INS) are key regions for integrating reward and surprise information, but conflicting evidence for both signed and unsigned activity has led to multiple proposals for the nature of RPE representations in these brain areas. Recently developed RL models allow neurons to respond differently to positive and negative RPEs. Here, we use intracranially recorded high frequency activity (HFA) to test whether this flexible asymmetric coding strategy captures RPE coding diversity in human INS and dMPFC. At the region level, we found a bias towards positive RPEs in both areas which paralleled behavioral adaptation. At the local level, we found spatially interleaved neural populations responding to unsigned RPE salience and valence-specific positive and negative RPEs. Furthermore, directional connectivity estimates revealed a leading role of INS in communicating positive and unsigned RPEs to dMPFC. These findings support asymmetric coding across distinct but intermingled neural populations as a core principle of RPE processing and inform theories of the role of dMPFC and INS in RL and cognitive control.

Authors:

• Colin W. Hoy

• David R. Quiroga-Martinez

• Eduardo Sandoval

• David King-Stephens

• Kenneth D. Laxer

• Peter Weber

• Jack J. Lin

• Robert T. Knight

Date: 2023

DOI: https://doi.org/10.1038/s41467-023-44248-1

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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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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

Authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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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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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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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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