Uncovering neuroanatomical correlates of impaired coordinated movement after pallidal deep brain stimulation

Background The loss of the ability to swim following deep brain stimulation (DBS), although rare, poses a worrisome risk of drowning. It is unclear what anatomic substrate and neural circuitry underlie this phenomenon. We report a case of cervical dystonia with lost ability to swim and dance during active stimulation of globus pallidus internus. We investigated the anatomical underpinning of this phenomenon using unique functional and structural imaging analysis. Methods Tesla (3T) functional MRI (fMRI) of the patient was used during active DBS and compared with a cohort of four matched patients without this side effect. Structural connectivity mapping was used to identify brain network engagement by stimulation. Results fMRI during stimulation revealed significant (Pbonferroni<0.0001) stimulation-evoked responses (DBS ON<OFF) in the supplementary motor area (SMA). Probabilistic tractography revealed that the patient’s VTAs engaged streamlines projecting to SMA. Compared with a cohort of matched controls, the stimulation-dependent change in blood oxygen level-dependent response at the SMA was 2.18 SD below the mean. Conclusions These stimulation-induced impairments are likely a manifestation of a broader deficit in interlimb coordination mediated by stimulation effects on the SMA. This neuroanatomical underpinning can help inform future patient-specific stimulation and targeting.