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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Consciousness is supported by near-critical slow cortical electrodynamics

Abstract:

Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, we empirically identify a mathematically specific critical point near which waking cortical oscillatory dynamics operate, which is known as the edge-of-chaos critical point, or the boundary between stability and chaos. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magnetoencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of low-frequency cortical electric oscillations away from this critical point; conversely, we show that psychedelics may increase the information richness of cortical activity by tuning low-frequency cortical oscillations closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC) and show that assessing the proximity of slow cortical oscillatory electrodynamics to the edge-of-chaos critical point may be useful as an index of consciousness in the clinical setting.

Authors:

• Daniel Toker

• Ioannis Pappas

• Janna D. Lendner

• Joel Frohlich

• Diego M. Mateos

• Suresh Muthukumaraswamy

• Robin Carhart-Harris

• Michelle Paff

• Paul M. Vespa

• Martin M. Monti

• Friedrich T. Sommer

• Robert T. Knight

• Mark D’Esposito

Date: 2022

DOI: https://doi.org/10.1073/pnas.2024455119

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Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

Abstract:

Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4–8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80–150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

Authors:

• Bradley Voytek

• Andrew S. Kayser

• David Badre

• David Fegen

• Edward F. Chang

• Nathan E. Crone

• Josef Parvizi

• Robert T. Knight

• Mark D'Esposito

Date: 2015

DOI: 10.1038/nn.4071

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A method for event-related phase/amplitude coupling

Authors:

• Bradley Voytek

• Mark D'Esposito

• Nathan E. Crone

• Robert T. Knight

Date: 2012

DOI: 10.1016/j.neuroimage.2012.09.023

PubMed: 22986076

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Abstract:

Phase/amplitude coupling (PAC) is emerging as an important electrophysiological measure of local and long-distance neuronal communication. Current techniques for calculating PAC provide a numerical index that represents an average value across an arbitrarily long time period. This requires researchers to rely on block design experiments and temporal concatenation at the cost of the sub-second temporal resolution afforded by electrophysiological recordings. Here we present a method for calculating event-related phase/amplitude coupling (ERPAC) designed to capture the temporal evolution of task-related changes in PAC across events or between distant brain regions that is applicable to human or animal electromagnetic recording.

Neural activity during social signal perception correlates with selfreported empathy

Authors:

• Christine I. Hooker

• Sara C. Verosky

• Laura T. Germine

• Robert T. Knight

• Mark D'Esposito

Date: 2010

DOI: 10.1016/j.brainres.2009.10.006

PubMed: 19836364

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Abstract:

Empathy is an important component of human relationships, yet the neural mechanisms that facilitate empathy are unclear. The broad construct of empathy incorporates both cognitive and affective components. Cognitive empathy includes mentalizing skills such as perspective-taking. Affective empathy consists of the affect produced in response to someone else's emotional state, a process which is facilitated by simulation or "mirroring." Prior evidence shows that mentalizing tasks engage a neural network which includes the temporoparietal junction, superior temporal sulcus, and medial prefrontal cortex. On the other hand, simulation tasks engage the fronto-parietal mirror neuron system (MNS) which includes the inferior frontal gyrus (IFG) and the somotosensory related cortex (SRC). Here, we tested whether neural activity in these two neural networks was related to self-reports of cognitive and affective empathy in daily life. Participants viewed social scenes in which the shift of direction of attention of a character did or did not change the character's mental and emotional state. As expected, the task robustly activated both mentalizing and MNS networks. We found that when detecting the character's change in mental and emotional state, neural activity in both networks is strongly related to cognitive empathy. Specifically, neural activity in the IFG, SRC, and STS were related to cognitive empathy. Activity in the precentral gyrus was related to affective empathy. The findings suggest that both simulation and mentalizing networks contribute to multiple components of empathy.

Mentalizing about emotion and its relationship to empathy

Authors:

• Christine I. Hooker

• Sara C. Verosky

• Laura T. Germine

• Robert T. Knight

• Mark D'Esposito

Date: 2008

DOI: 10.1093/scan/nsn019

PubMed: 19015112

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Abstract:

Mentalizing involves the ability to predict someone else’s behavior based on their belief state. More advanced mentalizing skills involve integrating knowledge about beliefs with knowledge about the emotional impact of those beliefs. Recent research indicates that advanced mentalizing skills may be related to the capacity to empathize with others. However, it is not clear what aspect of mentalizing is most related to empathy. In this study, we used a novel, advanced mentalizing task to identify neural mechanisms involved in predicting a future emotional response based on a belief state. Subjects viewed social scenes in which one character had a False Belief and one character had a True Belief. In the primary condition, subjects were asked to predict what emotion the False Belief Character would feel if they had a full understanding about the situation. We found that neural regions related to both mentalizing and emotion were involved when predicting a future emotional response, including the superior temporal sulcus, medial prefrontal cortex, temporal poles, somatosensory related cortices (SRC), inferior frontal gyrus and thalamus. In addition, greater neural activity in primarily emotion-related regions, including right SRC and bilateral thalamus, when predicting emotional response was significantly correlated with more self-reported empathy. The findings suggest that predicting emotional response involves generating and using internal affective representations and that greater use of these affective representations when trying to understand the emotional experience of others is related to more empathy.

Age-related top down suppression deficit in the early stages of cortical visual memory processing

Authors:

• Adam Gazzaley

• Wesley Clapp

• Jon Kelley

• Kevin McEvoy

• Robert T. Knight

• Mark D'Esposito

Date: 2008

DOI: 10.1073/pnas.0806074105

PubMed: 18765818

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Abstract:

In this study, electroencephalography (EEG) was used to examine the relationship between two leading hypotheses of cognitive aging, the inhibitory deficit and the processing speed hypothesis. We show that older adults exhibit a selective deficit in suppressing task-irrelevant information during visual working memory encoding, but only in the early stages of visual processing. Thus, the employment of suppressive mechanisms are not abolished with aging but rather delayed in time, revealing a decline in processing speed that is selective for the inhibition of irrelevant information. EEG spectral analysis of signals from frontal regions suggests that this results from excessive attention to distracting information early in the time course of viewing irrelevant stimuli. Subdividing the older population based on working memory performance revealed that impaired suppression of distracting information early in the visual processing stream is associated with poorer memory of task-relevant information. Thus, these data reconcile two cognitive aging hypotheses by revealing that an interaction of deficits in inhibition and processing speed contributes to agerelated cognitive impairment.

The influence of personality on neural mechanisms of observational fear and reward learning

Authors:

• Christine I. Hooker

• Sara C. Verosky

• Asako Miyakawa

• Robert T. Knight

• Mark D'Esposito

Date: 2008

DOI: 10.1016/j.neuropsychologia.2008.05.005

PubMed: 18573512

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Abstract:

Fear and reward learning can occur through direct experience or observation. Both channels can enhance survival or create maladaptive behavior. We used fMRI to isolate neural mechanisms of observational fear and reward learning and investigate whether neural response varied according to individual differences in neuroticism and extraversion. Participants learned object-emotion associations by observing a woman respond with fearful (or neutral) and happy (or neutral) facial expressions to novel objects. The amygdala–hippocampal complex was active when learning the object-fear association, and the hippocampus was active when learning the object-happy association. After learning, objects were presented alone; amygdala activity was greater for the fear (vs. neutral) and happy (vs. neutral) associated object. Importantly, greater amygdala–hippocampal activity during fear (vs. neutral) learning predicted better recognition of learned objects on a subsequent memory test. Furthermore, personality modulated neural mechanisms of learning. Neuroticism positively correlated with neural activity in the amygdala and hippocampus during fear (vs. neutral) learning. Low extraversion/high introversion was related to faster behavioral predictions of the fearful and neutral expressions during fear learning. In addition, low extraversion/high introversion was related to greater amygdala activity during happy (vs. neutral) learning, happy (vs. neutral) object recognition, and faster reaction times for predicting happy and neutral expressions during reward learning. These findings suggest that neuroticism is associated with an increased sensitivity in the neural mechanism for fear learning which leads to enhanced encoding of fear associations, and that low extraversion/high introversion is related to enhanced conditionability for both fear and reward learning.

Spatio-temporal dynamics of neural mechanisms underlying component operations in working memory

Authors:

• Brian T. Miller

• Leon Y. Deouell

• Cathrine Dam

• Robert T. Knight

• Mark D'Esposito

Date: 2008

DOI: 10.1016/j.brainres.2008.01.059

PubMed: 18358455

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Abstract:

Neuroimaging and neurophysiology evidence suggests that component operations in working memory (WM) emerge from the coordinated interaction of posterior perceptual cortices with heteromodal regions in the prefrontal and parietal cortices. Still, little is known about bottom– up and top–down signaling during the formation and retrieval of WM representations. In the current set of experiments, we combine complementary fMRI and EEG measures to obtain high-resolution spatial and temporal measures of neural activity during WM encoding and retrieval processes. Across both experiments, participants performed a face delayed recognition WM task in which the nature of sensory input across stages was held constant. In experiment 1, we utilized a latency-resolved fMRI approach to assess temporal parameters of the BOLD response during stage-specific encoding and retrieval waveforms. Relative to the latency at encoding, the PFC exhibited an earlier peak of fMRI activity at retrieval showing stage-specific differences in the temporal dynamics of PFC engagement across WM operations. In experiment 2, we analyzed the first 200 ms of the ERP response during this WM task providing a more sensitive temporal measure of these differences. Divergence of the ERP pattern during encoding and retrieval began as early as 60 ms post-stimulus. The parallel fMRI and ERP results during memory-guided decisions support a key role of the PFC in top–down biasing of perceptual processing and reveal rapid differences across WM component operations in the presence of identical bottom–up sensory input.

Cerebral responses to change in spatial location of unattended sounds

Authors:

• Leon Y. Deouell

• Aaron S. Heller

• Rafael Malach

• Mark D'Esposito

• Robert T. Knight

Date: 2007

DOI: 10.1016/j.neuron.2007.08.019

PubMed: 17880900

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Abstract:

The neural basis of spatial processing in the auditory cortex has been controversial. Human fMRI studies suggest that a part of the planum temporale (PT) is involved in auditory spatial processing, but it was recently argued that this region is active only when the task requires voluntary spatial localization. If this is the case, then this region cannot harbor an ongoing spa- tial representation of the acoustic environment. In contrast, we show in three fMRI experiments that a region in the human medial PT is sensitive to background auditory spatial changes, even when subjects are not engaged in a spatial lo- calization task, and in fact attend the visual mo- dality. During such times, this area responded to rare location shifts, and even more so when spatial variation increased, consistent with spatially selective adaptation. Thus, acoustic space is represented in the human PT even when sound processing is not required by the ongoing task.

Information analysis of event-related BOLD responses: exploring spatio-temporal patterns of brain activations

Authors:

• Galit Fuhrmann Alpert

• Fellice T. Sun

• Daniel Handwerker

• Mark D'Esposito

• Robert T. Knight

Date: 2007

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Amygdala response to facial expressions reflects emotional learning

Authors:

• Christine I. Hooker

• Laura T. Germine

• Robert T. Knight

• Mark D'Esposito

Date: 2006

PubMed: 16943547

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Abstract:

The functional role of the human amygdala in the evaluation of emotional facial expressions is unclear. Previous animal and human research shows that the amygdala participates in processing positive and negative reinforcement as well as in learning predictive associations between stimuli and subsequent reinforcement. Thus, amygdala response to facial expressions could reflect the processing of primary reinforcement or emotional learning. Here, using functional magnetic resonance imaging, we tested the hypothesis that amygdala response to facial expressions is driven by emotional association learning. We show that the amygdala is more responsive to learning object-emotion associations from happy and fearful facial expressions than it is to the presentation of happy and fearful facial expressions alone. The results provide evidence that the amygdala uses social signals to rapidly and flexibly learn threatening and rewarding associations that ultimately serve to enhance survival.

Controlling the integration of emotion and cognition: the role of frontal cortex in distinguishing helpful from hurtful emotional information

Authors:

• Jennifer S. Beer

• Robert T. Knight

• Mark D'Esposito

Date: 2006

PubMed: 16683934

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Abstract:

Emotion has been both lauded and vilified for its role in decision making. How are people able to ensure that helpful emotions guide decision making and irrelevant emotions are kept out of decision making? The orbitofrontal cortex has been identified as a neural area involved in incorporating emotion into decision making. Is this area's function specific to the integration of emotion and cognition, or does it more broadly govern whether emotional information should be integrated into cognition? The present research examined the role of orbitofrontal cortex when it was appropriate to control (i.e., prevent) the influence of emotion in decision making (Experiment 1) and to incorporate the influence of emotion in decision making (Experiment 2). Together, the two studies suggest that activity in lateral orbitofrontal cortex is associated with evaluating the contextual relevance of emotional information for decision making.

Top-down enhancement and suppression of the magnitude and speed of neural activity

Authors:

• Adam Gazzaley

• Jeffrey W. Cooney

• Kevin McEvoy

• Robert T. Knight

• Mark D'Esposito

Date: 2005

PubMed: 15814009

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Abstract:

Top-down modulation underlies our ability to selectively attend to relevant stimuli and to ignore irrelevant stimuli. Theories addressing neural mechanisms of top-down modulation are driven by studies that reveal increased magnitude of neural activity in response to directed attention, but are limited by a lack of data reporting modulation of neural processing speed, as well as comparisons with a perceptual (passive view) baseline necessary to evaluate the presence of enhancement and suppression. Utilizing functional MRI (fMRI) and event-related potential recordings (ERPs), we provide converging evidence that both the magnitude of neural activity and the speed of neural processing are modulated by top-down influences. Furthermore, both enhancement and suppression occur relative to a perceptual baseline depending on task instruction. These findings reveal the fine degree of influence that goal-directed attention exerts upon activity within the visual association cortex. We further document capacity limitations in top-down enhancement corresponding with working memory performance deficits.

Rapid Prefrontal-Hippocampal Habituation to Novel Events

Authors:

• Shuhei Yamaguchi

• Laura A. Hale

• Mark D'Esposito

• Robert T. Knight

Date: 2004

PubMed: 15190108

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Abstract:

Unexpected novel events generate an orienting response that plays an important role in some forms of learning and memory. The orienting response involuntarily captures attention and rapidly habituates as events become familiarized. Although evidence from patients with focal lesions and scalp and intracranial event-related brain potential recordings supports the involvement of a distributed neural network involving association cortex and the limbic system in novelty detection, the key neural substrates and temporal dynamics have not been defined. While subjects performed a bi-field visual-selective attention task with random novel stimuli embedded in either attended or unattended visual fields, we measured rapid changes of regional blood oxygenation level-dependent (BOLD) signal to target and novel stimuli using single-trial analysis of event-related functional magnetic resonance imaging with a 4T scanner. Habituation was quantified by serial BOLD signal changes during the first 10 novel stimuli for each subject. Novel stimuli activated the bilateral superior/middle frontal gyrus, temporal-parietal junction, superior parietal lobe, cingulate gyrus, hippocampus, and fusiform gyrus. The superior/middle frontal gyrus and hippocampus showed significant reduction of BOLD signal during the first few novel stimuli, whereas the signals in the fusiform and cingulate gyrus were constant. Prefrontal and hippocampal responses to attended and unattended novel stimuli were comparably habituated. These results, and previous data from lesion studies, support the view that prefrontal and hippocampal regions are involved in rapid automatic detection and habituation to unexpected environmental events and are key elements of the orienting response in humans.

Lateral prefrontal syndrome: a disorder of executive control

Authors:

• Robert T. Knight

• Mark D'Esposito

Date: 2003

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Effects of frontal lobe damage on interference effects in working memory

Authors:

• Sharon L. Thompson-Schill

• John Jonides

• Christy Marshuetz

• Edward E. Smith

• Mark D'Esposito

• Irene P. Kan

• Robert T. Knight

• Diane Swick

Date: 2002

PubMed: 12455679

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Abstract:

Working memory is hypothesized to comprise a collection of distinct components or processes, each of which may have a unique neural substrate. Recent neuroimaging studies have isolated a region of the left inferior frontal gyrus that appears to be related specifically to one such component: resolving interference from previous items in working memory. In the present study, we examined working memory in patients with unilateral frontal lobe lesions by using a modified version of an item recognition task in which interference from previous trials was manipulated. In particular, we focused on patient R.C., whose lesion uniquely impinged on the region identified in the neuroimaging studies of interference effects. We measured baseline working memory performance and interference effects in R.C. and other frontal patients and in age-matched control subjects and young control subjects. Comparisons of each of these groups supported the following conclusions. Normal aging is associated with changes to both working memory and interference effects. Patients with frontal damage exhibited further declines in working memory but normal interference effects, with the exception of R.C., who exhibited a pronounced interference effect on both response time and accuracy. We propose that the left inferior frontal gyrus subserves a general, nonmnemonic function of selecting relevant information in the face of competing alternatives and that this function may be required by some working memory tasks.

Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings

Authors:

• Sharon L. Thompson-Schill

• Diane Swick

• Martha J. Farah

• Mark D'Esposito

• Irene P. Kan

• Robert T. Knight

Date: 1998

PubMed: 9861060

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Abstract:

What are the neural bases of semantic mem- ory? Traditional beliefs that the temporal lobes subserve the retrieval of semantic knowledge, arising from lesion studies, have been recently called into question by functional neuro- imaging studies finding correlations between semantic re- trieval and activity in left prefrontal cortex. Has neuroimag- ing taught us something new about the neural bases of cognition that older methods could not reveal or has it merely identified brain activity that is correlated with but not caus- ally related to the process of semantic retrieval? We examined the ability of patients with focal frontal lesions to perform a task commonly used in neuroimaging experiments, the gen- eration of semantically appropriate action words for concrete nouns, and found evidence of the necessity of the left inferior frontal gyrus for certain components of the verb generation task. Notably, these components did not include semantic retrieval per se.