Asymmetric transcallosal conduction delay leads to finer bimanual coordination

Abstract

It has been theorized that hemispheric dominance and more segregated information processing have evolved to overcome long conduction delays through the corpus callosum (transcallosal conduction delay-TCD) but that this may still impact behavioral performance, mostly in tasks requiring high timing accuracy. Nevertheless, a thorough understanding of the temporal features of interhemispheric communication is lacking. Here, we aimed to assess the relationship between TCD and behavioral performance with a noninvasive directional cortical measure of TCD obtained from transcranial magnetic stimulation (TMS)evoked potentials (TEPs) in the motor system. Twenty-one healthy right-handed subjects were tested. TEPs were recorded during an ipsilateral silent period (iSP) paradigm and integrated with diffusion tensor imaging (DTI) and an in-phase bimanual thumb-opposition task. Linear mixed models were applied to test relationships between measures. We found TEP indexes of transcallosal communication at~15 ms both after primary motor cortex stimulation (M1-P15) and after dorsal premotor cortex stimulation (dPMC-P15). Both M1-and dPMC-P15 were predicted by mean diffusivity in the callosal body. Moreover, M1-P15 was positively related to iSP. Importantly, M1-P15 latency was linked to bimanual coordination with direction-dependent effects, so that asymmetric TCD was the best predictor of bimanual coordination. Our findings support the idea that transcallosal timing in signal transmission is essential for interhemispheric communication and can impact the final behavioral outcome. However, they challenge the view that a short conduction delay is always beneficial. Rather, they suggest that the effect of the conduction delay may depend on the direction of information flow.

Reliability of M1-P15 as a cortical marker for transcallosal inhibition: a preregistered TMS-EEG study

“…In our recent study [19], we combined TMS-EEG with diffusion tensor imaging (DTI), which provides microstructural information on callosal integrity, and with the ipsilateral silent period (iSP), a wellknown peripheral measure of interhemispheric inhibition obtained from TMS and electromyography [20]. Our results provided first evidence of M1-P15, a positive component occurring approximately 15 ms after M1 stimulation, as a TEP-derived measure of transcallosal inhibition between motor cortices.…”

“…The bimanual coordination tasks involved a metronome-paced in-phase movements at 2 Hz: a repetitive mirror-symmetrical thumb-to-index opposition task (Tapping) and a sequential mirrorsymmetrical thumb-to-finger opposition task (Sequence), as in [19,27]. Specifically, in the Sequence task participants were asked to oppose their thumb to the other fingers, in the following order: index, middle, ring and little finger.…”

“…Finally, we calculated the normalized iSP area using the following formula [(area of the rectangle defined as mean EMG x iSP duration)−(area underneath the iSP)]. Then, the normalized iSP area was defined as the ratio between the iSP area and the area underneath EMG from -150 to 50 ms preceding TMS [19,32]. Even if the number of trials considered for iSP calculation are consistent with the iSP literature, they represent only a subset of the trials presented and that were considered for M1-P15 calculation.…”

An integrated TMS-EEG and MRI approach to explore the interregional connectivity of the default mode network

“…Therefore, even in the absence of task-related neuronal activation and "specific" external input, all these synchronized brain regions form resting-state networks (van den Heuvel and Hulshoff Pol 2010). This high level of functional connectivity between regions suggests the existence of a distinctive brain structural architecture to facilitate such ongoing interregional communication (Boorman et al 2007;Bortoletto et al 2021;Momi et al 2021;Quentin et al 2015;Silverstein et al 2020). Thus, understanding how to measure such dynamic patterns underlying brain functions is one of the crucial questions in neuroscience.…”

“…The majority of studies on brain connectivity have been obtained from stand-alone unimodal neuroimaging methods (Plis et al 2011). We proposed the use of an integrative approach with a combination of different methods (Bergmann et al 2016) composed of structural and functional magnetic resonance imaging (MRI and fMRI, respectively), diffusion-weighted imaging (DWI), and transcranial magnetic stimulation and electroencephalography (TMS-EEG) coregistration (Bortoletto et al 2021;Esposito et al 2020;Levy-Lamdan et al 2020;Momi et al 2021;Voineskos et al 2010).…”