Introduction Increasing evidence from functional brain imaging and cortical mapping with transcranial magnetic stimulation (TMS) supports the hypothesis that human swallowing shows hemispheric asymmetry in the motor cortex. However, the physiological and neuroanatomical relevance of this asymmetry remains controversial. We aimed to apply complimentary imaging modalities in-vivo, to evaluate the neuroanatomical connections that contribute to the cerebral control of swallowing using TMS, functional magnetic resonance imaging (fMRI), diffusion weighted imaging (DWI) and probabilistic tractography.
Methods In six healthy adults (5M/1F, 27–37 years) TMS evoked pharyngeal motor responses, recorded via a swallowed intraluminal catheter, were used to assess the motor cortical representation of swallowing in both hemispheres. Thereafter, two 8-min fMRI scans were performed using a Philips Achieva 3-T scanner to assess changes in blood-oxygenation-level-dependent signals in response to water swallowing. Each run consisted of alternating 1 minute “on” (12 swallows) and “off” (no swallowing) periods in a block-trial design. Distortion-corrected DWI data were then acquired for probabilistic tractography to determine anatomical fibre tracts. Swallowing-related fMRI activations were identified using FSL and used to seed unconstrained multifibre PICo tractography independently in each hemisphere. These results were compared with TMS inter-hemispheric differences.
Results TMS data revealed 5/6 subjects had hemispheric dominance for swallowing (2 left, 3 right). FMRI data revealed asymmetric activations in both sensorimotor cortices in each subject which were used as seed regions for tractography. Paired t-test revealed significantly larger patterns of connectivity in the TMS predicted dominant projection compared to the non-dominant projection (p<0.03). Tractography displayed consistently larger tract volumes in the dominant motor cortex (p<0.03). Fibre tracking identified multiple connections between swallowing motor cortex and regions known to be involved in the control of swallowing including cingulate cortex, insula, supplementary and pre-motor areas. The dominant projection was also more strongly connected to regions transcallosally than the non-dominant projection.
Conclusion Our study applied multimodal imaging to explore in detail the neuroanatomy of human swallowing and quantify fibre tracts within the cortical swallowing network. Our data provide further evidence for cerebral asymmetry in the control of swallowing, supporting the notion that asymmetry seen with brain imaging is biologically relevant.
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