Six-dimensional dynamic tractography atlas of language connectivity in the developing brain

Abstract

During a verbal conversation, our brain moves through a series of complex linguistic processing stages: sound decoding, semantic comprehension, retrieval of semantically coherent words, and overt production of speech outputs. Each process is thought to be supported by a network consisting of local and long-range connections bridging between major cortical areas. Both temporal and extratemporal lobe regions have functional compartments responsible for distinct language domains, including the perception and production of phonological and semantic components. This study provides quantitative evidence of how directly connected inter-lobar neocortical networks support distinct stages of linguistic processing across brain development. Novel six-dimensional tractography was used to intuitively visualize the strength and temporal dynamics of direct inter-lobar effective connectivity between cortical areas activated during each linguistic processing stage. We analysed 3401 non-epileptic intracranial electrode sites from 37 children with focal epilepsy (aged 5–20 years) who underwent extra-operative electrocorticography recording. Principal component analysis of auditory naming-related high-gamma modulations determined the relative involvement of each cortical area during each linguistic processing stage. To quantify direct effective connectivity, we delivered single-pulse electrical stimulation to 488 temporal and 1581 extratemporal lobe sites and measured the early cortico-cortical spectral responses at distant electrodes. Mixed model analyses determined the effects of naming-related high-gamma co-augmentation between connecting regions, age, and cerebral hemisphere on the strength of effective connectivity independent of epilepsy-related factors. Direct effective connectivity was strongest between extratemporal and temporal lobe site pairs, which were simultaneously activated between sentence offset and verbal response onset (i.e. response preparation period); this connectivity was approximately twice more robust than that with temporal lobe sites activated during stimulus listening or overt response. Conversely, extratemporal lobe sites activated during overt response were equally connected with temporal lobe language sites. Older age was associated with increased strength of inter-lobar effective connectivity especially between those activated during response preparation. The arcuate fasciculus supported approximately two-thirds of the direct effective connectivity pathways from temporal to extratemporal auditory language-related areas but only up to half of those in the opposite direction. The uncinate fasciculus consisted of <2% of those in the temporal-to-extratemporal direction and up to 6% of those in the opposite direction. We, for the first time, provided an atlas which quantifies and animates the strength, dynamics, and direction specificity of inter-lobar neural communications between language areas via the white matter pathways. Language-related effective connectivity may be strengthened in an age-dependent manner even after the age of 5.

Dynamic tractography‐based localization of spike sources and animation of spike propagations

“…49 Nonetheless, we have recently demonstrated that the velocity of SPES-induced neural propagations was highly comparable between the opensource and individual DWI data. 35 One should consider the effect of volume conduction when electrode sites >10 mm apart exhibit an identical waveform without a time delay. 50 Based on the visual assessment, we believe that the unwanted effect of volume conduction on our iEEG analysis was small.…”

“…As previously performed, 14,35 we generated DWI tractography using the open‐source data averaged across the 1065 individuals participating in the Human Connectome Project (http://brain.labsolver.org/diffusion-mri-templates/hcp-842-hcp-1021). 36 We validated our analytic approach by demonstrating that the spatial patterns of SPES‐induced neural propagations based on the open‐source DWI data were similar to those based on the individual data 35 …”

“…36 We validated our analytic approach by demonstrating that the spatial patterns of SPES-induced neural propagations based on the opensource DWI data were similar to those based on the individual data. 35 We placed seed-spheres of a radius of 4 mm at leading, lagging, and perilesional cortical sites. Within the MNI space, DSI Studio (http://dsi-studio.labso lver.org/) generated streamlines between the leading and lagging sites in all 19 patients.…”

Temporally and functionally distinct large-scale brain network dynamics supporting task switching

“…Considering the various iEEG frequency bands ranging from alpha through high-gamma, event-related high-gamma augmentation was reported to best predict the severity of cognitive deficits following focal brain resection ( Sonoda et al, 2022 ). Diffusion-weighted imaging (DWI) tractography can visualize the direct white matter tracts allowing neural communications between distant cortical regions concurrently involved in a cognitive process ( Sonoda et al, 2021 ). The present study elucidated the spatiotemporal dynamics and functional significance of iEEG-derived neural modulations during task switching by addressing the following aims.…”

“…We performed this analysis to provide the biological plausibility for direct functional connectivity between distant cortical areas concurrently involved in task switching. It is suggested that cognitive processes are supported by spatially-distinct, simultaneous high-frequency neural events generated by monosynaptically connected cortical networks ( Singer, 1993 , 2018 ; Buonomano and Merzenich, 1998 ; Sonoda et al, 2021 ).…”