Homology and Specificity of Natural Sound-Encoding in Human and Monkey Auditory Cortex

Abstract

Understanding homologies and differences in auditory cortical processing in human and nonhuman primates is an essential step in elucidating the neurobiology of speech and language. Using fMRI responses to natural sounds, we investigated the representation of multiple acoustic features in auditory cortex of awake macaques and humans. Comparative analyses revealed homologous large-scale topographies not only for frequency but also for temporal and spectral modulations. In both species, posterior regions preferably encoded relatively fast temporal and coarse spectral information, whereas anterior regions encoded slow temporal and fine spectral modulations. Conversely, we observed a striking interspecies difference in cortical sensitivity to temporal modulations: While decoding from macaque auditory cortex was most accurate at fast rates (> 30 Hz), humans had highest sensitivity to ~3 Hz, a relevant rate for speech analysis. These findings suggest that characteristic tuning of human auditory cortex to slow temporal modulations is unique and may have emerged as a critical step in the evolution of speech and language.

Temporal selectivity declines in the aging human auditory cortex

“…Although the large scale topographic organization of acoustic features appears preserved in the auditory cortex of older compared to younger listeners, age-related differences in the marginal profiles of multi-voxel MTFs were evident. Tuning to slow temporal rates which abounds in natural sounds and especially in speech (Erb et al, 2018) was markedly sharper in young compared to older participants. Consistent with previous findings in the macaque, these results suggest that temporal rate selectivity in auditory cortex declines in normal aging.…”

“…While previous studies had presented single natural sounds (Erb et al, 2018), or even synthetic sounds such as AM stimuli (Baumann et al, 2015) or dynamic ripples (Schonwiesner and Zatorre, 2009), here, we presented a continuous stream of speech embedded in an acoustically rich background of sound textures. As an important foundation for the main conclusions of this manuscript, we here demonstrate the capacity to derive meaningful tonotopic maps from natural stimulus conditions, at conventional field strengths (3 T) and in special populations (older participants).…”

“…We applied a computational modelling approach to fMRI data as described in Erb et al (2018). Two modelling procedures were applied (Fig.…”

“…Recent advances in computational modelling of fMRI data has led to substantial progress in our understanding of how natural sounds become represented in the auditory cortex. A series of studies have shown that cortical processing of sounds is optimized to represent the spectro-temporal modulations which are typically present in conspecific vocalizations such as speech or animal calls (Santoro et al, 2014, Hullett et al, 2016, Santoro et al, 2017, Erb et al, 2018). However, those models have not looked at the pressing case of the aged human cortex.…”

Aberrant perceptual judgements on speech-relevant acoustic features in hallucination-prone individuals

“…To date, it is unclear in how far the general response properties of auditory cortex are altered in voice hearers. A recent strain of research provides converging evidence that the healthy human auditory cortex analyzes sounds along so-called spectro-temporal modulations: The auditory pathway is thought to not only implement forms of “tonotopic” frequency analysis 18 , but to rather represent sound as frequency-specific spectral and temporal modulation filters 19,20 for neurobiological evidence see e.g., 21,22 ). Hallucinations in schizophrenia have been linked to deficits in object formation 23 .…”