Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain's functional architecture

Hutchison, R. Matthew; Hutchison, Melina; Manning, Kathryn Y.; Menon, Ravi S.; Everling, Stefan

doi:10.1002/hbm.22583

Cited by 135 publications

(150 citation statements)

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“…The effects of isoflurane, the most commonly used anesthetic in monkeys, could be reflected as changes in the correlation strength between brain areas, localization, or inclusion of distributed nodes within specific networks (19,28). However, recent research has shown that within a carefully controlled narrow range of isoflurane levels, such as 6 .26% in our study, statistical coupling between brain areas was consistent and reliable for investigation of functional brain architecture (19,26). Moreover, we argue the potential effect of anesthetic agents was removed by contrasting the saline and ketamine treatments in the same group subjects and the thresholds for network construction were applied uniformly to each subject in both conditions.…”

Section: Regional Regulation Of Small-world Networkmentioning

confidence: 51%

“…Growing evidence has validated the use of restingstate functional magnetic resonance imaging (rsfMRI) in anesthetized macaques (19)(20)(21)(22)(23)(24)(25)(26)(27) and has underscored its potential to bridge information between human and animal models (28)(29)(30)(31). Although the effect of anesthetic agents on functional brain networks remains poorly understood, recent study has demonstrated that stable functional connectivity patterns under a narrow range of medium level isoflurane (e.g., 6.25%) are suitable for anesthetized nonhuman primate investigations (26). Furthermore, whole-brain rsfMRI allows unbiased, simultaneous identification of all pharmacologically affected regions in the brain.…”

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confidence: 99%

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Large-Scale Persistent Network Reconfiguration Induced by Ketamine in Anesthetized Monkeys: Relevance to Mood Disorders

Yang

et al. 2016

Biological Psychiatry

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Section: Regional Regulation Of Small-world Networkmentioning

confidence: 51%

mentioning

confidence: 99%

Large-Scale Persistent Network Reconfiguration Induced by Ketamine in Anesthetized Monkeys: Relevance to Mood Disorders

Yang

et al. 2016

Biological Psychiatry

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“…The macaque fMRI data were acquired under low-dose anesthesia, and although this method is known to produce robust patterns of FC that are homologous to human FC networks (57), it may affect the temporal structure of FC at higher doses (58). Interhemispheric FC, in particular, is vulnerable to isoflurane in a dose-dependent fashion (59), and this vulnerability may explain why the difference in FC strength between intrahemispheric and heterotopic connections was more pronounced in the macaque than in the human dataset. Future studies using fMRI acquired in awake animals will be needed to investigate cross-species differences in interhemispheric coordination more directly.…”

Section: Discussionmentioning

confidence: 99%

Stable long-range interhemispheric coordination is supported by direct anatomical projections

Shen¹,

Mišić

Cipollini

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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119

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The functional interaction between the brain's two hemispheres includes a unique set of connections between corresponding regions in opposite hemispheres (i.e., homotopic regions) that are consistently reported to be exceptionally strong compared with other interhemispheric (i.e., heterotopic) connections. The strength of homotopic functional connectivity (FC) is thought to be mediated by the regions' shared functional roles and their structural connectivity. Recently, homotopic FC was reported to be stable over time despite the presence of dynamic FC across both intrahemispheric and heterotopic connections. Here we build on this work by considering whether homotopic FC is also stable across conditions. We additionally test the hypothesis that strong and stable homotopic FC is supported by the underlying structural connectivity. Consistent with previous findings, interhemispheric FC between homotopic regions were significantly stronger in both humans and macaques. Across conditions, homotopic FC was most resistant to change and therefore was more stable than heterotopic or intrahemispheric connections. Across time, homotopic FC had significantly greater temporal stability than other types of connections. Temporal stability of homotopic FC was facilitated by direct anatomical projections. Importantly, temporal stability varied with the change in conductive properties of callosal axons along the anterior-posterior axis. Taken together, these findings suggest a notable role for the corpus callosum in maintaining stable functional communication between hemispheres.functional connectivity | structural connectivity | homotopy | dynamics T he brain's capacity for processing information relies on a modular and hierarchical functional architecture that allows both functional segregation and integration (1, 2). Distributed processing occurs within segregated communities responsible for highly specialized functions, whereas more comprehensive functions require long-range integration across communities. This long-range integration is especially important for coordinating functions between the two hemispheres. Functional connectivity (FC), computed as the temporal correlation or covariance between regionwise signals, varies across different interhemispheric regions. FC is significantly stronger between homotopic regions than between heterotopic regions (3) and is greater than would be expected from the anatomical distance between the homotopic regions (4). This strong homotopic FC is thought to be mediated by the strong underlying structural connectivity of the corpus callosum (CC). Indeed, the majority of callosal fibers are between homotopic brain regions (5-7), and the loss of callosal integrity leads to a loss in homotopic FC (8, 9).Recently, a growing number of resting-state functional MRI (fMRI) studies have reported how FC varies over time (10). Flexibility in cognitive processing is thought to arise from the ability of certain regions to participate dynamically in different network configurations (11). For instance, ...

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“…First, data were obtained under anesthesia to both maintain stable physiological conditions and to limit head movement. The resting-state fMRI signal in rats, as in other species (50,51), appears to be anesthetic dependent (52,53). However, Grandjean et al (51) suggested that the combined use of medetomidine and isoflurane maintains strong correlations within both cortical and subcortical structures in mice.…”

Section: Modulation Of Dmn Connectivity As a Function Of Age-relatedmentioning

confidence: 99%

Constituents and functional implications of the rat default mode network

Hsu

Liang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

100

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The default mode network (DMN) has been suggested to support a variety of self-referential functions in humans and has been fractionated into subsystems based on distinct responses to cognitive tasks and functional connectivity architecture. Such subsystems are thought to reflect functional hierarchy and segregation within the network. Because preclinical models can inform translational studies of neuropsychiatric disorders, partitioning of the DMN in nonhuman species, which has previously not been reported, may inform both physiology and pathophysiology of the human DMN. In this study, we sought to identify constituents of the rat DMN using resting-state functional MRI (rs-fMRI) and diffusion tensor imaging. After identifying DMN using a group-level independent-component analysis on the rs-fMRI data, modularity analyses fractionated the DMN into an anterior and a posterior subsystem, which were further segregated into five modules. Diffusion tensor imaging tractography demonstrates a close relationship between fiber density and the functional connectivity between DMN regions, and provides anatomical evidence to support the detected DMN subsystems. Finally, distinct modulation was seen within and between these DMN subcomponents using a neurocognitive aging model. Taken together, these results suggest that, like the human DMN, the rat DMN can be partitioned into several subcomponents that may support distinct functions. These data encourage further investigation into the neurobiological mechanisms of DMN processing in preclinical models of both normal and disease states.default mode network | functional connectivity | modularity | rat brain | aging T he default mode network (DMN) of the brain, first demonstrated in humans (1) and then in nonhuman primates (2) and rodents (3-5), contains a set of distributed brain regions that are approximately analogous across the species. Anatomically, the human DMN includes medial prefrontal cortex (mPFC), anterior cingulate cortex (ACC), posterior cingulate cortex (PCC) and precuneus, bilateral inferior parietal cortex, temporal cortex, and hippocampus (HIPP) (6, 7). The human DMN is thought to support a variety of self-referential functions, including recollection and imagination, conceptual processing, and autobiographical memory (6,8,9). A reduction of DMN's activity (or deactivation) has been conceptualized as the suppression of brain activity responsible for processing introspective thinking and planning. In so doing, it supports the processing of events external to the individual, including such executive functions as working memory (10). Compared with healthy individuals, various neurological and psychiatric disorders including schizophrenia (11), Alzheimer's disease (12), autism (13), and addiction (14, 15) have been linked to DMN dysregulation.Based on distinct responses to various cognitive tasks and functional connectivity architecture, the human DMN has been fractionated using both graph theory (16) and independentcomponent analysis (ICA) methods (17) into a set of...

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Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain's functional architecture

Cited by 135 publications

References 113 publications

Large-Scale Persistent Network Reconfiguration Induced by Ketamine in Anesthetized Monkeys: Relevance to Mood Disorders

Large-Scale Persistent Network Reconfiguration Induced by Ketamine in Anesthetized Monkeys: Relevance to Mood Disorders

Stable long-range interhemispheric coordination is supported by direct anatomical projections

Constituents and functional implications of the rat default mode network

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