Multimodal neuroimaging characteristics of sleep-related painful erections: a resting-state fMRI and voxel-based...

Sleep-related painful erections (SRPE) are a rare parasomnia featuring recurrent nocturnal awakenings from painful penile erections, with daytime erections remaining painless; their central neural mechanisms remain poorly characterized.

To delineate the structural and functional neuroimaging signatures of SRPE using multimodal cerebral magnetic resonance imaging (MRI).

Twenty-two men with SRPE and 23 age-matched healthy men (HCs) underwent structural and resting-state functional MRI. Grey matter volume (GMV) was compared using voxel-based morphometry (VBM), and regional spontaneous activity using the fractional amplitude of low-frequency fluctuations (fALFF). VBM and fALFF clusters served as seeds for whole-brain seed-to-voxel and region-of-interest-to-region-of-interest (ROI-to-ROI) functional connectivity (FC). All imaging analyses were corrected for multiple comparisons at P < .05 (peak-level family-wise-error for VBM; cluster-level false-discovery-rate for fALFF and seed-to-voxel FC; threshold-free cluster enhancement for ROI-to-ROI FC). Sensitivity analyses adjusted each finding individually for erectile function, premature ejaculation, anxiety, and depression.

Primary outcomes were between-group differences in GMV, fALFF, and FC; secondary outcomes were correlations between altered imaging metrics and clinical features.

Relative to HCs, SRPE patients showed reduced GMV in the bilateral putamen, right posterior orbitofrontal cortex, and bilateral superior temporal gyri (STG). fALFF was decreased in the right inferior temporal gyrus and the left middle occipital gyrus and increased in the left orbital superior frontal gyrus; this increase correlated negatively with the Pittsburgh Sleep Quality Index (r = -0.499, P < .001) and SRPE frequency (r = -0.616, P = .002) but did not survive adjustment for erectile function. Seed-to-voxel FC was increased between the bilateral STG and the anterior cingulate cortex (ACC), the left putamen and left middle temporal gyrus, and the left middle and superior occipital gyri. ROI-to-ROI analysis showed increased connectivity of the bilateral ACC and right midcingulate cortex with the left central operculum, left Heschl's gyrus, and bilateral STG. The right-hemisphere structural findings, the reduced-fALFF findings, and the bilateral STG-ACC hyperconnectivity were robust to all covariates; left-hemisphere and intra-occipital effects were not.

These findings offer preliminary evidence of central nervous system involvement in SRPE that may eventually inform neuromodulation-based approaches.

This is the first multimodal cerebral MRI study of SRPE. Limitations include the modest sample, cross-sectional design, absence of sleep-state recording, and comorbidities that preclude causal and fully specific inference.

Multimodal MRI identified associative structural and functional alterations in regions implicated in pain processing, sleep regulation, and affective-cognitive integration in SRPE.