Rupp, K. | Search bioRxiv

bioRxiv2021

Categorical encoding of voice in human superior temporal cortex

The ability to recognize abstract features of voice during auditory perception is a complex, yet poorly understood, feat of human audition. For the listener, this occurs in near-automatic fasion to seamlessly extract complex cues from a highly variable auditory signal. Voice perception depends on specialized regions of auditory cortex, including superior temporal gyrus (STG) and superior temporal sulcus (STS). However, the nature of voice encoding at the cortical level remains poorly understoood. We leverage intracerebral recordings across human auditory cortex during presentation of voice and non-voice acoustic stimuli to examine voice encoding in auditory cortex, in eight patient-participants undergoing epilepsy surgery evaluation. We show that voice-selectivity increases along the auditory hierarchy from supratemporal plane (STP) to the STG and STS. Results show accurate decoding of vocalizations from human auditory cortical activity even in the complete absence of linguistic content. These findings show an early, less-selective temporal window of neural activity in the STG and STS followed by a sustained, strongly voice-selective window. We then developed encoding models that demonstrate divergence in the encoding of acoustic features along the auditory hierarchy, wherein STG/STS responses were best explained by voice category as opposed to the acoustic features of voice stimuli. This is in contrast to neural activity recorded from STP, in which responses were accounted for by acoustic features. These findings support a model of voice perception that engages categorical encoding mechanisms within STG and STS. Significance StatementVoice perception occurs via specialized networks in higher order auditory cortex, yet how voice features are encoded remains a central unanswered question. With human intracerebral recordings of auditory cortex, we provide evidence for categorical encoding of voice in STG and STS and occurs in the absence of linguistic content. This selectivity strengthens after an initial onset response and cannot be explained by simple acoustic features. Together, these data support the existence of sites within STG and STS that are specialized for voice perception.

neuroscience↗

bioRxiv2021

Deconstructing the Cortical Sources of Frequency Following Responses to Speech: A Cross-species Approach

Time-varying pitch is a vital cue for human speech perception. Neural processing of time-varying pitch has been extensively assayed using scalp-recorded frequency-following responses (FFRs), an electrophysiological signal thought to reflect integrated phase-locked neural ensemble activity from subcortical auditory areas. Emerging evidence increasingly points to a putative contribution of auditory cortical ensembles to the scalp-recorded FFRs. However, the properties of cortical FFRs and precise characterization of laminar sources are still unclear. Here we used direct human intracortical recordings as well as extra- and intracranial recordings from macaques and guinea pigs to characterize the properties of cortical sources of FFRs to time-varying pitch patterns. We found robust FFRs in the auditory cortex across all species. We leveraged representational similarity analysis as a translational bridge to characterize similarities between the human and animal models. Laminar recordings in animal models showed FFRs emerging primarily from the thalamorecepient layers of the auditory cortex. FFRs arising from these cortical sources significantly contributed to the scalp-recorded FFRs via volume conduction. Our research paves the way for a wide array of studies to investigate the role of cortical FFRs in auditory perception and plasticity. Significance StatementFrequency following responses (FFRs) to speech are scalp-recorded neural signals that inform the fidelity of sound encoding in the auditory system. FFRs, long believed to arise from brainstem and midbrain, have shaped our understanding of sub-cortical auditory processing and plasticity. Non-invasive studies have shown cortical contributions to the FFRs, however, this is still actively debated. Here we employed direct cortical recordings to trace the cortical contribution to the FFRs and characterize the properties of these cortical FFRs. With extra-cranial and intra-cranial recordings within the same subjects we show that cortical FFRs indeed contribute to the scalp-recorded FFRs, and their response properties differ from the sub-cortical FFRs. The findings provide strong evidence to revisit and reframe the FFR driven theories and models of sub-cortical auditory processing and plasticity with careful characterization of cortical and sub-cortical components in the scalp-recorded FFRs.

neuroscience↗