The autonomic brain: Multi-dimensional generative hierarchical modelling of the autonomic connectome

Ruffle, James K.; Hyare, Harpreet; Howard, Matthew A.; Farmer, Adam D.; Apkarian, A. Vania; Williams, Steven; Aziz, Qasim; Nachev, Parashkev

doi:10.1016/j.cortex.2021.06.012

Cited by 20 publications

(30 citation statements)

References 61 publications

(79 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These findings substantiate the claim that the bilateral anterior insula cortex, the midcingulate cortex, and the bilateral inferior parietal lobule, with small regions of the bilateral middle frontal gyrus, constitute a single robust functional network supporting a central representation of the autonomic systems. Inconsistent with assumptions of previous work, our results do not provide meta-analytic support either for the presence of divergent networks underlying sympathetic and parasympathetic systems (Beissner et al, 2013) or for a robust involvement of the default mode network in central processing of autonomic activity (Beissner et al, 2013;Nagai et al, 2004;Thayer et al, 2012), in particular parasympathetic activity (Babo-Rebelo et al, 2016;Ruffle et al, 2021). These results, however, should be taken with caution because they may be due to the effects of the relatively low number of studies investigating the parasympathetic system (12%) compared with studies investigating the sympathetic system (44%) and the sympathetic/parasympathetic system (44%), making our results more consistent with the central processing network of sympathetic activity.…”

Section: Discussioncontrasting

confidence: 67%

The central autonomic system revisited – convergent evidence for a regulatory role of the insular and midcingulate cortex from neuroimaging meta-analyses

Ferraro

Klugah‐Brown

Tench

et al. 2022

Preprint

View full text Add to dashboard Cite

The autonomic nervous system regulates dynamic body adaptations to internal and external environment changes. Capitalizing on two different algorithms (Analysis of Brain Coordinates and GingerALE) that differ in empirical assumptions, we scrutinized the meta-analytic convergence of human neuroimaging studies investigating the neural basis of peripheral autonomic signal processing. Among the selected studies, we identified 42 records reporting 44 different experiments and testing 792 healthy individuals.The results of the two different algorithms converge in identifying the bilateral dorsal anterior insula and midcingulate cortex as the critical areas of the central autonomic system (CAN). However, whereas the bilateral dorsal anterior insula appears to be involved in processing autonomic nervous system signals regardless of task type, activity in the midcingulate cortex appears to be primarily engaged in processing autonomic signals during cognitive tasks and task-free conditions. Applying an unbiased approach, we were able to identify a single functionally condition-independent circuit that supports CAN activity. Although partially overlapping with the salience network, this functional circuit includes, in addition to the bilateral insular cortex and midcingulate cortex, the bilateral inferior parietal lobules and small clusters in the bilateral middle frontal gyrus. Our results do not support the hypothesis of divergent pathways for the sympathetic and parasympathetic systems or a robust involvement of the default mode network, particularly during parasympathetic activity. However, these results may be due to the relatively low number of studies investigating the parasympathetic system (12%), making our results more consistent with the central processing network of sympathetic activity.Remarkably, the critical regions of the CAN observed in this meta-analysis are among the most reported co-activated areas in neuroimaging studies and have been repeatedly shown as being dysregulated across different mental and neurological disorders. This suggests that the central dynamic interaction maintaining bodily homeostasis reported in several brain imaging studies may be associated with increased autonomic nervous system engagement and that disruptions in this interplay may underpin unspecific pathological symptoms across mental and neurological disorders.

show abstract

Section: Discussioncontrasting

confidence: 67%

The central autonomic system revisited – convergent evidence for a regulatory role of the insular and midcingulate cortex from neuroimaging meta-analyses

Ferraro

Klugah‐Brown

Tench

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Having initialised a fit, we used simulated annealing to further optimise it, with a default inverse temperature of 1 to 10. 96 We did not specify a finite number of draws, rather we specified a wait step of 100 iterations for a record-breaking event, to ensure that equilibration was driven by changes in the entropy criterion, instead of driven by a finite number of iterations 102…”

Section: Methodsmentioning

confidence: 99%

Graph lesion-deficit mapping of fluid intelligence

Cipolotti

Ruffle

Mole

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

Fluid intelligence is arguably the defining feature of human cognition. Yet the nature of its relationship with the brain remains a contentious topic. Influential proposals drawing primarily on functional imaging data have implicated "multiple demand" frontoparietal and more widely distributed cortical networks, but extant lesion-deficit studies with greater causal power are almost all small, methodologically constrained, and inconclusive. The task demands large samples of patients, comprehensive investigation of performance, fine-grained anatomical mapping, and robust lesion-deficit inference, yet to be brought to bear on it. We assessed 165 healthy controls and 227 frontal or non-frontal patients with unilateral brain lesions on the best-established test of fluid intelligence, Raven's Advanced Progressive Matrices, employing an array of lesion-deficit inferential models responsive to the potentially distributed nature of fluid intelligence. Non-parametric Bayesian stochastic block models were used to reveal the community structure of lesion deficit networks, disentangling functional from confounding pathological distributed effects. Impaired performance was confined to patients with frontal lesions (F(2,387) = 18.491; p < .001; frontal worse than non-frontal and healthy participants p < .01; p <.001), more marked on the right than left (F(4,385) = 12.237; p < .001; right worse than left and healthy participants p<.01; p<.001). Patients with non-frontal lesions were indistinguishable from controls and showed no modulation by laterality. Neither the presence nor the extent of multiple demand network involvement affected performance. Both conventional network-based statistics and non-parametric Bayesian stochastic block modelling heavily implicated the right frontal lobe. Crucially, this localisation was confirmed on explicitly disentangling functional from pathology-driven effects within a layered stochastic block model, prominently highlighting a right frontal network involving middle and inferior frontal gyrus, pre- and post-central gyri, with a weak contribution from right superior parietal lobule. Similar results were obtained with standard lesion-deficit analyses. Our study represents the first large-scale investigation of the distributed neural substrates of fluid intelligence in the focally injured brain. Combining novel graph-based lesion-deficit mapping with detailed investigation of cognitive performance in a large sample of patients provides crucial information about the neural basis of intelligence. Our findings indicate that a set of predominantly right frontal regions, rather than a more widely distributed network, is critical to the high-level functions involved in fluid intelligence. Further they suggest that Raven's Advanced Progressive Matrices is a useful clinical index of fluid intelligence and a sensitive marker of right frontal lobe dysfunction.

show abstract

“…were evaluated using meta-analytic functional maps derived from natural language processing of published imaging studies. This was achieved with NeuroQuery image search matching[56] in a framework similar to other published approaches[57]. Passing each identified significant ROI from Bayesian structural imaging models to the NeuroQuery repository of 13,459 studies encompassing 5,144 activation pattern terms, we retrieved the closest matching 10 topic terms.…”

Section: Methodsmentioning

confidence: 99%

“…Cognitive implications from structural brain changes were evaluated using meta-analytic functional maps derived from natural language processing of published imaging studies. This was achieved with NeuroQuery image search matching [56] in a framework similar to other published approaches [57]. Passing each identified significant ROI from Bayesian structural imaging models to the NeuroQuery repository of 13,459 studies encompassing 5,144 activation pattern terms, we retrieved the closest matching 10 topic terms.…”

Section: Post-hoc Analyses Of Functional Connectivity Network Were Un...mentioning

confidence: 99%

Changes in brain structure and function in a multisport cohort of retired female and male athletes, many years after suffering a concussion. The ICHIRF-BRAIN Study

Turner

Belli

Castellani³

et al. 2022

Preprint

View full text Add to dashboard Cite

Mild traumatic brain injury is widely regarded as a misnomer: it is globally a major cause of disability and is hypothesized as a potential causal factor in subsequent neurodegeneration. Commonly arising in sport, mounting evidence of varying degrees of cognitive impairment in retired athletes exposed to repeated concussions motivates close examination of its cumulative effects on the brain. Studying a cohort of 125 retired athletes with a mean of 11 reported concussions and 36 matched controls with none, here we evaluated whole-brain volumetric and subcortical morphological effects with Bayesian regression models and functional connectivity effects with network-based statistics. Estimates of potential cognitive impact were derived from meta-analytic functional mapping based on 13,459 imaging studies. Across the array of brain structural and functional effects identified, regions significantly lower in volume in the concussed group included, in order of greatest effect size, the middle frontal gyrus, hippocampus, supramarginal gyrus, temporal pole, and inferior frontal gyrus. Conversely, brain regions significantly larger within the athlete group included, in order of greatest effect size, the hippocampal and collateral sulcus, middle occipital gyrus, medial orbital gyrus, caudate nucleus, lateral orbital gyrus, and medial segment to the postcentral gyrus (all significant with 95% Bayesian credible interval). Subcortical morphology analysis corroborated these findings, revealing a significant, age-independent relationship between inward deformation of the hippocampus and the number of concussions sustained (corrected- p<0.0001). Functional connectivity analyses revealed a distinct brain network with significantly increased edge strength in the athlete cohort comprising 150 nodes and 400 edges (corrected-p=0.02), with the highest degree nodes including the pre-central and post-central gyri and right insula. The functional communities of the greatest eigenvector centralities corresponded to motor domains. Numerous edges of this network strengthened in athletes were significantly weakened with increasing bouts of concussion, which included disengagement of the frontal pole, superior frontal, and middle frontal gyri (p=0.04). Aligned to meta-analytic neuroimaging data, the observed changes suggest possible functional enhancement within the motor, sensory, coordination, balance, and visual processing domains in athletes, attenuated by concussive head injury with a negative impact on memory and language. That such changes are observed many years after retirement from impact sport suggests strong repetition effects and/or underpinning genetic selection factors. These findings suggest that engagement in sport may benefit the brain across numerous domains, but also highlights the potentially damaging effects of concussive head injury.

show abstract

The autonomic brain: Multi-dimensional generative hierarchical modelling of the autonomic connectome

Cited by 20 publications

References 61 publications

The central autonomic system revisited – convergent evidence for a regulatory role of the insular and midcingulate cortex from neuroimaging meta-analyses

The central autonomic system revisited – convergent evidence for a regulatory role of the insular and midcingulate cortex from neuroimaging meta-analyses

Graph lesion-deficit mapping of fluid intelligence

Changes in brain structure and function in a multisport cohort of retired female and male athletes, many years after suffering a concussion. The ICHIRF-BRAIN Study

Contact Info

Product

Resources

About