Myogenic artifacts masquerade as neuroplasticity in the auditory frequency-following response

Abstract

The frequency-following response (FFR) is an evoked potential that provides a neural index of complex sound encoding in the brain. FFRs have been widely used to characterize speech and music processing, experience-dependent neuroplasticity (e.g., learning and musicianship), and biomarkers for hearing and language-based disorders that distort receptive communication abilities. It is widely assumed that FFRs stem from a mixture of phase-locked neurogenic activity from the brainstem and cortical structures along the hearing neuraxis. In this study, we challenge this prevailing view by demonstrating that upwards of ~50% of the FFR can originate from an unexpected myogenic source: contamination from the postauricular muscle (PAM) vestigial startle reflex. We measured PAM, transient auditory brainstem responses (ABRs), and sustained frequency-following response (FFR) potentials reflecting myogenic (PAM) and neurogenic (ABR/FFR) responses in young, normal-hearing listeners with varying degrees of musical training. We first establish that PAM artifact is present in all ears, varies with electrode proximity to the muscle, and can be experimentally manipulated by directing listeners' eye gaze toward the ear of sound stimulation. We then show this muscular noise easily confounds auditory FFRs, spuriously amplifying responses 3–4-fold with tandem PAM contraction and even explaining putative FFR enhancements observed in highly skilled musicians. Our findings expose a new and unrecognized myogenic source to the FFR that drives its large inter-subject variability and cast doubt on whether changes in the response typically attributed to neuroplasticity/pathology are solely of brain origin.