Heterogeneity of trans-callosal structural connectivity and effects on resting state subnetwork integrity may underlie both wanted and unwanted effects of therapeutic corpus callostomy.

Peter Neal Taylor,Rob Forsyth

doi:10.1016/j.nicl.2016.07.010

Peter Neal Taylor, Rob Forsyth

Open Access

https://doi.org/10.1016/j.nicl.2016.07.010

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Abstract

BackgroundThe corpus callosum (CC) is the primary structure supporting interhemispheric connectivity in the brain. Partial or complete surgical callosotomy may be performed for the palliation of intractable epilepsy. A variety of disconnection syndromes are recognised after injury to or division of the CC however their mechanisms are poorly understood and their occurrence difficult to predict. We use novel high resolution structural connectivity analyses to demonstrate reasons for this poor predictability.MethodsDiffusion weighted MRI data from five healthy adult controls was subjected to novel high-resolution structural connectivity analysis. We simulated the effects of CC lesions of varying extents on the integrity of resting state subnetworks (RSNs).ResultsThere is substantial between-individual variation in patterns of CC connectivity. However in all individuals termination points of callosal connections mostly involve medial and superior sensory-motor areas. Superior temporal and lateral sensory-motor areas were not involved. Resting state networks showed selective vulnerability to simulated callosotomy of progressively greater anterior to posterior extent. The default mode network was most vulnerable followed by, in decreasing order: frontoparietal, limbic, somatomotor, ventral attention, dorsal attention and visual subnetworks.ConclusionConsideration of the selective vulnerability of resting state sub-networks, and of between-individual variability in connectivity patterns, sheds new light on the occurrence of both wanted and unwanted effects of callosotomy. We propose that beneficial effects (seizure reduction) relate to disruption of the default mode network, with unwanted “disconnection syndrome” effects due to disruption particularly of the somatomotor and frontoparietal RSNs. Our results may also explain why disconnection syndromes primary reflect lateralised sensory-motor problems (e.g. of limb movement) rather than midline function (e.g. tongue movement). Marked between-subject variation in callosal connectivity may underlie the poor predictability of effects of callosotomy. High resolution structural connectivity studies of this nature may be useful in pre-surgical planning of therapeutic callosotomy for intractable epilepsy.

Highlights

The corpus callosum (CC)1 is the major anatomical structure supporting inter-hemispheric connectivity in the brain
Since tractography uses random initial conditions, we examined the reproducibility of the tractography and subsequent processing, repeating the entire pipeline using the same data
Diffusion Tensor Imaging (DTI)-based structural connectivity studies of the CC have been performed previously (Molko et al, 2002; Lebel et al, 2010; Benezit et al, 2015), the spatial resolution achieved in this study, dividing the cortical surface into over 104 surface region of interest (ROI), is unprecedented

Summary

Introduction

The corpus callosum (CC) is the major anatomical structure supporting inter-hemispheric connectivity in the brain It may be congenitally absent (Benezit et al, 2015), or callosal disconnection can be acquired as a result of traumatic brain injury (Basu et al, 2015). A range of disconnection syndromes have been described following partial or complete callosotomy These include the supplementary motor area (SMA) syndrome, the anarchic (or alien) hand syndrome, tactile dysnomia, hemispatial neglect, non-dominant hand agraphia and alexia without agraphia (for review see Jea et al (2008)). We propose that beneficial effects (seizure reduction) relate to disruption of the default mode network, with unwanted “disconnection syndrome” effects due to disruption of the somatomotor and frontoparietal RSNs. Our results may explain why disconnection syndromes primary reflect lateralised sensory-motor problems (e.g. of limb movement) rather than midline function (e.g. tongue movement). High resolution structural connectivity studies of this nature may be useful in pre-surgical planning of therapeutic callosotomy for intractable epilepsy

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