Revisiting ‘brain modes’ in a new computational era: approaches for the characterization of brain-behavioural associations

Toba, Monica N.; Godefroy, Olivier; Rushmore, R. Jarrett; Zavaglia, Melissa; Maatoug, Redwan; Hilgetag, Claus C.; Valero‐Cabré, Antoni

doi:10.1093/brain/awz343

Cited by 33 publications

(26 citation statements)

References 77 publications

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“…Second, using the MSA approach on mean disconnection values for each individual white matter bundle, we were unable to document situations in which similar deficits were induced by lesions on different locations along the trajectory of a bundle, thus to describe very common situations observed in clinical settings, whereby two separate lesions may give rise to the same deficit (see the so‐called “equivalence” brain‐mode reported by Godefroy et al () and revisited recently in Toba et al, ; see also Toba et al, ). This situation should be given particular attention in the future.…”

Section: Discussionmentioning

confidence: 99%

Game theoretical mapping of white matter contributions to visuospatial attention in stroke patients with hemineglect

Toba

Zavaglia

Malherbe

et al. 2020

Human Brain Mapping

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White matter bundles linking gray matter nodes are key anatomical players to fully characterize associations between brain systems and cognitive functions. Here we used a multivariate lesion inference approach grounded in coalitional game theory (multiperturbation Shapley value analysis, MSA) to infer causal contributions of white matter bundles to visuospatial orienting of attention. Our work is based on the characterization of the lesion patterns of 25 right hemisphere stroke patients and the causal analysis of their impact on three neuropsychological tasks: line bisection, letter cancellation, and bells cancellation. We report that, out of the 11 white matter bundles included in our MSA coalitions, the optic radiations, the inferior fronto‐occipital fasciculus and the anterior cingulum were the only tracts to display task‐invariant contributions (positive, positive, and negative, respectively) to the tasks. We also report task‐dependent influences for the branches of the superior longitudinal fasciculus and the posterior cingulum. By extending prior findings to white matter tracts linking key gray matter nodes, we further characterize from a network perspective the anatomical basis of visual and attentional orienting processes. The knowledge about interactions patterns mediated by white matter tracts linking cortical nodes of attention orienting networks, consolidated by further studies, may help develop and customize brain stimulation approaches for the rehabilitation of visuospatial neglect.

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Section: Discussionmentioning

confidence: 99%

Game theoretical mapping of white matter contributions to visuospatial attention in stroke patients with hemineglect

Toba

Zavaglia

Malherbe

et al. 2020

Human Brain Mapping

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“…Paradoxical lesion effects are intriguing functional phenomena that have attracted much attention and controversy [ 43 , 44 ]. How were paradoxical lesion effects produced in our example network?…”

Section: Discussionmentioning

confidence: 99%

Systematic perturbation of an artificial neural network: A step towards quantifying causal contributions in the brain

Fakhar

Hilgetag

2022

PLoS Comput Biol

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Lesion inference analysis is a fundamental approach for characterizing the causal contributions of neural elements to brain function. This approach has gained new prominence through the arrival of modern perturbation techniques with unprecedented levels of spatiotemporal precision. While inferences drawn from brain perturbations are conceptually powerful, they face methodological difficulties. Particularly, they are challenged to disentangle the true causal contributions of the involved elements, since often functions arise from coalitions of distributed, interacting elements, and localized perturbations have unknown global consequences. To elucidate these limitations, we systematically and exhaustively lesioned a small artificial neural network (ANN) playing a classic arcade game. We determined the functional contributions of all nodes and links, contrasting results from sequential single-element perturbations with simultaneous perturbations of multiple elements. We found that lesioning individual elements, one at a time, produced biased results. By contrast, multi-site lesion analysis captured crucial details that were missed by single-site lesions. We conclude that even small and seemingly simple ANNs show surprising complexity that needs to be addressed by multi-lesioning for a coherent causal characterization.

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“…Information on acute treatment or the pre-stroke level of stroke was furthermore not readily available for the entire cohort. As recommended in the literature, 62 we computed continuous values for region-wise lesion status (i.e., we calculated how many voxels were damaged per region), rather than applying a binarizing damage threshold. Nonetheless, we focused on a binary outcome – favorable versus unfavorable outcomes – and continuous, more granular and domain-specific outcome measures may facilitate even more detailed insights, as outlined above.…”

Section: Discussionmentioning

confidence: 99%

The relevance of rich club regions for functional outcome post-stroke is enhanced in women

Bonkhoff

Schirmer

Bretzner

et al. 2022

Preprint

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This study aimed to investigate the influence of stroke lesions in pre-defined highly interconnected (rich club) brain regions on functional outcome post-stroke, determine their spatial specificity and explore the effects of biological sex on their relevance. We analyzed MRI data recorded at index stroke and ~3-months modified Rankin Scale (mRS) data from patients with acute ischemic stroke (AIS) enrolled in the multisite MRI-GENIE study. Structural stroke lesions were spatially normalized and parcellated into 108 atlas-defined bilateral (sub)cortical brain regions. Unfavorable outcome (mRS>2) was modeled in a Bayesian logistic regression framework that relied on both lesion location, as well as the covariates: age, sex, total DWI lesion volume and comorbidities. Effects of individual brain regions were captured as two compound effects for (i) six bilateral rich club and (ii) all further non-rich club regions. Via model comparisons, we first tested whether the rich club region model was superior to a baseline model considering clinical covariates and lesion volume only. In spatial specificity analyses, we randomized the split into rich club and non-rich club regions and compared the effect of the actual rich club regions to the distribution of effects from 1,000 combinations of six random regions. In sex-specific analyses, we introduced an additional hierarchical level in our model structure to compare male and female-specific rich club region effects. A total of 822 patients (age: 64.7 (standard deviation: 15.0), 39% women, 27.7% with mRS>2) were analyzed. The rich club model substantially outperformed the baseline model (weights of model comparison: rich club model: 0.96; baseline: 0.04). Rich club regions had substantial relevance in explaining unfavorable functional outcome (mean of posterior distribution: 0.08, area under the curve: 0.8). In particular, the rich club-combination had a higher relevance than 98.4% of random constellations (15/1,000 random constellations with higher mean posterior values). Among the these 15 random constellations with higher means, the most frequently selected regions were the inferior temporal gyrus (posterior division, 8/15), the putamen (8/15), the cingulate gyrus (7/15) and the superior parietal lobule (6/15). Rich club regions were substantially more important in explaining long-term outcome in women than in men (mean of the difference distribution:-0.107, 90%-HDPI:-0.193 to -0.0124). Lesions in rich club regions were associated with increased odds of unfavorable outcome. These effects were spatially specific, i.e., the majority of random combinations of six regions had comparably smaller effects on long-term outcome. Effects were substantially more pronounced in women.

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Revisiting ‘brain modes’ in a new computational era: approaches for the characterization of brain-behavioural associations

Cited by 33 publications

References 77 publications

Game theoretical mapping of white matter contributions to visuospatial attention in stroke patients with hemineglect

Game theoretical mapping of white matter contributions to visuospatial attention in stroke patients with hemineglect

Systematic perturbation of an artificial neural network: A step towards quantifying causal contributions in the brain

The relevance of rich club regions for functional outcome post-stroke is enhanced in women

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