Neural generators of the frequency-following response elicited to stimuli of low and high frequency: A magnetoencephalographic (MEG) study

Abstract

The frequency-following response (FFR) to periodic complex sounds has gained recent interest in auditory cognitive neuroscience as it captures with great fidelity the tracking accuracy of the periodic sound features in the ascending auditory system. Seminal studies suggested the FFR as a correlate of subcortical sound encoding, yet recent studies aiming to locate its sources challenged this assumption, demonstrating that FFR receives some contribution from the auditory cortex. Based on frequency-specific phase-locking capabilities along the auditory hierarchy, we hypothesized that FFRs to higher frequencies would receive less cortical contribution than those to lower frequencies, hence supporting a major subcortical involvement for these high frequency sounds. Here, we used a magnetoencephalographic (MEG) approach to trace the neural sources of the FFR elicited in healthy adults (N = 19) to low (89 Hz) and high (333 Hz) frequency sounds. FFRs elicited to the high and low frequency sounds were clearly observable on MEG and comparable to those obtained in simultaneous electroencephalographic recordings. Distributed source modeling analyses revealed midbrain, thalamic, and cortical contributions to FFR, arranged in frequency-specific configurations. Our results showed that the main contribution to the high-frequency sound FFR originated in the inferior colliculus and the medial geniculate body of the thalamus, with no significant cortical contribution. In contrast, the low-frequency sound FFR had a major contribution located in the auditory cortices, and also received contributions originating in the midbrain and thalamic structures. These findings support the multiple generator hypothesis of the FFR and are relevant for our understanding of the neural encoding of sounds along the auditory hierarchy, suggesting a hierarchical organization of periodicity encoding.