Transient Suppression of Broadband Gamma Power in the Default-Mode Network Is Correlated with Task Complexity and Subject Performance

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358

Information processing during human cognitive and emotional operations is thought to involve the dynamic interplay of several large-scale neural networks, including the fronto-parietal central executive network (CEN), cingulo-opercular salience network (SN), and the medial prefrontal-medial parietal default mode networks (DMN). It has been theorized that there is a causal neural mechanism by which the CEN/SN negatively regulate the DMN. Support for this idea has come from correlational neuroimaging studies; however, direct evidence for this neural mechanism is lacking. Here we undertook a direct test of this mechanism by combining transcranial magnetic stimulation (TMS) with functional MRI to causally excite or inhibit TMS-accessible prefrontal nodes within the CEN or SN and determine consequent effects on the DMN. Single-pulse excitatory stimulations delivered to only the CEN node induced negative DMN connectivity with the CEN and SN, consistent with the CEN/SN's hypothesized negative regulation of the DMN. Conversely, low-frequency inhibitory repetitive TMS to the CEN node resulted in a shift of DMN signal from its normally low-frequency range to a higher frequency, suggesting disinhibition of DMN activity. Moreover, the CEN node exhibited this causal regulatory relationship primarily with the medial prefrontal portion of the DMN. These findings significantly advance our understanding of the causal mechanisms by which major brain networks normally coordinate information processing. Given that poorly regulated information processing is a hallmark of most neuropsychiatric disorders, these findings provide a foundation for ways to study network dysregulation and develop brain stimulation treatments for these disorders. task positive network | task negative network | fMRI | neuromodulation E xtensive neuroimaging work has described a set of largescale, intrinsically organized networks in the human brain, as well as those of other mammals, which are thought to underlie a broad range of functions, from basic sensory and motor capacities to cognition and higher-level functions (1-4). Three networks in particular have been the focus of work related to these higher-level functions (5): the fronto-parietal central executive network (CEN), the cingulo-opercular salience network (SN), and the medial prefrontal-medial parietal default mode network (DMN). These networks are thought to interact and together control attention, working memory, decision making, and other higher-level cognitive operations (6-8).Findings to date, however, emphasize the need for a direct test of the proposed causal relationship between these networks. On the basis of observations in resting-state functional MRI (rsfMRI) scans in humans of time-locked negative CEN/DMN and SN/DMN connectivity (9-11), as well as mathematical modeling of temporal relationships between these networks (12), it has been argued that the CEN and/or SN negatively regulate activity in the DMN. However, because a similar pattern of connectivity can be spuriously introduced du...

Section: Discussionmentioning

confidence: 56%

Causal interactions between fronto-parietal central executive and default-mode networks in humans

Chen

Oathes

Chang

et al. 2013

509

358

“…Furthermore, this suppression in firing rate is correlated with behavioral performance, where lower levels of PCC firing suppression are associated with longer reaction times (RTs) and higher error rate, a correlation also previously reported with fMRI in humans (11,12). Similarly, direct cortical recordings using electrocorticography (ECoG) from human DMN (13)(14)(15)(16) have shown suppression of broadband γ-power [a correlate of population firing rate (17,18)] during attentional effort. More recently, this broadband suppression across human DMN regions has also been shown to correlate with behavioral performance (16).…”

mentioning

confidence: 54%

“…Event-related changes in spectral power were initially screened for a wide range of frequencies and then more specifically for band-limited changes. For functional electrode selection and the bulk of analysis reported, we focused on the event-related changes in broad-frequency high γ-power (HG; 70-180 Hz), as used by previous investigators (13,15,16). Changes in power across this frequency range reflect one of the most robust measures of local population activity as recorded by ECoG, particularly given that power in this range is functionally selective, spatially restricted (20), and well-correlated with both population firing rate (17) and fMRI responses (21).…”

Section: Resultsmentioning

confidence: 99%

“…Similarly, direct cortical recordings using electrocorticography (ECoG) from human DMN (13)(14)(15)(16) have shown suppression of broadband γ-power [a correlate of population firing rate (17,18)] during attentional effort. More recently, this broadband suppression across human DMN regions has also been shown to correlate with behavioral performance (16). Taken together, these findings have provided clear electrophysiological evidence for DMN suppression.…”

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confidence: 99%

See 1 more Smart Citation

Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing

Foster

Dastjerdi

Parvizi

2012

102

Our understanding of the human default mode network derives primarily from neuroimaging data but its electrophysiological correlates remain largely unexplored. To address this limitation, we recorded intracranially from the human posteromedial cortex (PMC), a core structure of the default mode network, during various conditions of internally directed (e.g., autobiographical memory) as opposed to externally directed focus (e.g., arithmetic calculation). We observed late-onset (>400 ms) increases in broad high γ-power (70-180 Hz) within PMC subregions during memory retrieval. High γ-power was significantly reduced or absent when subjects retrieved self-referential semantic memories or responded to selfjudgment statements, respectively. Conversely, a significant deactivation of high γ-power was observed during arithmetic calculation, the duration of which correlated with reaction time at the signaltrial level. Strikingly, at each recording site, the magnitude of activation during episodic autobiographical memory retrieval predicted the degree of suppression during arithmetic calculation. These findings provide important anatomical and temporal details-at the neural population level-of PMC engagement during autobiographical memory retrieval and address how the same populations are actively suppressed during tasks, such as numerical processing, which require externally directed attention.electrocorticography | episodic memory | numerical cognition O ur ability to successfully direct and maintain attention to the external world relies on the coordinated activation of several putative attentional brain networks. Over the past decade brain imaging techniques, such as functional MRI (fMRI), have also revealed a select group of brain regions, now well-known as the default mode network (DMN), which deactivate during tasks of externally directed attention (1, 2). Conversely, the DMN shows higher activity during tasks requiring internally focused "self-referential" processing (3-5). Despite the many advances made by neuroimaging studies of DMN function, similar progress in the electrophysiological domain has remained relatively limited. This scarcity of investigation is mostly because the core structures of the DMN are anatomically hidden on the medial surface of the brain, and thus their location and orientation is suboptimal for detection with scalp electroencephalography (EEG). One region of particular interest is the posteromedial cortex (PMC), which is the main hub of the DMN in the human (2, 6) and nonhuman primate (7, 8) brains (Fig. 1), and encompasses the posterior cingulate cortex (PCC), retrosplenial cortex (RSC), precuneus, and Brodmann area 31 (9). Ultimately, more invasive techniques using intracranial electrophysiological recordings from the human brain are methodologically preferable for studying these regions, but obtaining such data has been rare and logistically challenging.Recent invasive electrophysiological studies of the DMN have highlighted its well-known deactivation during conditions of externally d...

“…Indeed a consistent finding related to DMN cortical deactivation during cognitive task performance is a transient suppression of the gamma band, which is time-locked to the onset of task performance and varies in amplitude in relation to task difficulty (21)(22)(23)(24). Conversely, gamma-band activity is elevated in human DMN structures during control conditions that include quiet wakefulness, fixating one's eyes on a target, or an eyes-closed condition.…”

Section: Significancementioning

confidence: 93%

Basal forebrain contributes to default mode network regulation

Nair

Klaassen

Arató³

et al. 2018

The default mode network (DMN) is a collection of cortical brain regions that is active during states of rest or quiet wakefulness in humans and other mammalian species. A pertinent characteristic of the DMN is a suppression of local field potential gamma activity during cognitive task performance as well as during engagement with external sensory stimuli. Conversely, gamma activity is elevated in the DMN during rest. Here, we document that the rat basal forebrain (BF) exhibits the same pattern of responses, namely pronounced gamma oscillations during quiet wakefulness in the home cage and suppression of this activity during active exploration of an unfamiliar environment. We show that gamma oscillations are localized to the BF and that gamma-band activity in the BF has a directional influence on a hub of the rat DMN, the anterior cingulate cortex, during DMNdominated brain states. The BF is well known as an ascending, activating, neuromodulatory system involved in wake-sleep regulation, memory formation, and regulation of sensory information processing. Our findings suggest a hitherto undocumented role of the BF as a subcortical node of the DMN, which we speculate may be important for switching between internally and externally directed brain states. We discuss potential BF projection circuits that could underlie its role in DMN regulation and highlight that certain BF nuclei may provide potential target regions for up-or down-regulation of DMN activity that might prove useful for treatment of DMN dysfunction in conditions such as epilepsy or major depressive disorder.gamma suppression | anterior cingulate cortex | granger causality A highly consistent finding across a wide range of functional imaging studies in humans is that a network of brain regions, referred to as the "default mode network" (DMN), increases its activity during passive mental states compared with the performance of cognitive tasks. This was initially shown in a metaanalysis of several PET studies (1), in which a distribution of brain regions broadly including the medial prefrontal, retrosplenial, and anterior cingulate cortex (ACC), as well as lateral parietal and temporal cortices, was shown to be activated when subjects were in a state of quiet restfulness. The DMN areas are thought to form a cohesive set of intrinsically coupled brain regions, such that fMRI activations in its component regions exhibit similar time courses, allowing them to be identified reliably using seed-region analysis (2-4). Activity in the DMN exhibits anticorrelation with a complementary, largely nonoverlapping, set of fronto-parietal brain areas known as the "dorsal attention network" (DAN) (5). It should be noted, however, that particular brain structures may harbor functionally heterogeneous elements and thus may contribute to multiple functions, as was shown for the ACC (6). During wakefulness, the human brain thus alternates between DAN-and DMN-dominated activation states, corresponding to effortful cognitive task performance on the one hand and quiet restful...