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Primary auditory cortex is a critical stage in the human auditory pathway, a gateway between subcortical and higher-level cortical areas. Receiving the output of all subcortical processing, it sends its output on to higher-level cortex. Non-invasive physiological recordings of primary auditory cortex using electroencephalography (EEG) and magnetoencephalography (MEG), however, may not have sufficient specificity to separate responses generated in primary auditory cortex from those generated in underlying subcortical areas or neighboring cortical areas. This limitation is important for investigations of effects of top-down processing (e.g., selective-attention-based) on primary auditory cortex: higher-level areas are known to be strongly influenced by top-down processes, but subcortical areas are often assumed to perform strictly bottom-up processing. Fortunately, recent advances have made it easier to isolate the neural activity of primary auditory cortex from other areas. In this perspective, we focus on time-locked responses to stimulus features in the high gamma band (70–150 Hz) and with early cortical latency (∼40 ms), intermediate between subcortical and higher-level areas. We review recent findings from physiological studies employing either repeated simple sounds or continuous speech, obtaining either a frequency following response (FFR) or temporal response function (TRF). The potential roles of top-down processing are underscored, and comparisons with invasive intracranial EEG (iEEG) and animal model recordings are made. We argue that MEG studies employing continuous speech stimuli may offer particular benefits, in that only a few minutes of speech generates robust high gamma responses from bilateral primary auditory cortex, and without measurable interference from subcortical or higher-level areas.
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Subcortical responses to music and speech are alike while cortical responses diverge
Music and speech are encountered daily and are unique to human beings. Both are transformed by the auditory pathway from an initial acoustical encoding to higher level cognition. Studies of cortex have revealed distinct brain responses to music and speech, but differences may emerge in the cortex or may be inherited from different subcortical encoding. In the first part of this study, we derived the human auditory brainstem response (ABR), a measure of subcortical encoding, to recorded music and speech using two analysis methods. The first method, described previously and acoustically based, yielded very different ABRs between the two sound classes. The second method, however, developed here and based on a physiological model of the auditory periphery, gave highly correlated responses to music and speech. We determined the superiority of the second method through several metrics, suggesting there is no appreciable impact of stimulus class (i.e., music vs speech) on the way stimulus acoustics are encoded subcortically. In this study’s second part, we considered the cortex. Our new analysis method resulted in cortical music and speech responses becoming more similar but with remaining differences. The subcortical and cortical results taken together suggest that there is evidence for stimulus-class dependent processing of music and speech at the cortical but not subcortical level.
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- Award ID(s):
- 2142612
- PAR ID:
- 10523884
- Publisher / Repository:
- Scientific Reports
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Aging is associated with an exaggerated representation of the speech envelope in auditory cortex. The relationship between this age-related exaggerated response and a listener’s ability to understand speech in noise remains an open question. Here, information-theory-based analysis methods are applied to magnetoencephalography recordings of human listeners, investigating their cortical responses to continuous speech, using the novel nonlinear measure of phase-locked mutual information between the speech stimuli and cortical responses. The cortex of older listeners shows an exaggerated level of mutual information, compared with younger listeners, for both attended and unattended speakers. The mutual information peaks for several distinct latencies: early (∼50 ms), middle (∼100 ms), and late (∼200 ms). For the late component, the neural enhancement of attended over unattended speech is affected by stimulus signal-to-noise ratio, but the direction of this dependency is reversed by aging. Critically, in older listeners and for the same late component, greater cortical exaggeration is correlated with decreased behavioral inhibitory control. This negative correlation also carries over to speech intelligibility in noise, where greater cortical exaggeration in older listeners is correlated with worse speech intelligibility scores. Finally, an age-related lateralization difference is also seen for the ∼100 ms latency peaks, where older listeners show a bilateral response compared with younger listeners’ right lateralization. Thus, this information-theory-based analysis provides new, and less coarse-grained, results regarding age-related change in auditory cortical speech processing, and its correlation with cognitive measures, compared with related linear measures. NEW & NOTEWORTHY Cortical representations of natural speech are investigated using a novel nonlinear approach based on mutual information. Cortical responses, phase-locked to the speech envelope, show an exaggerated level of mutual information associated with aging, appearing at several distinct latencies (∼50, ∼100, and ∼200 ms). Critically, for older listeners only, the ∼200 ms latency response components are correlated with specific behavioral measures, including behavioral inhibition and speech comprehension.more » « less
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Abstract Several methods have recently been developed to derive the auditory brainstem response (ABR) from continuous natural speech, facilitating investigation into subcortical encoding of speech. These tools rely on deconvolution to compute the temporal response function (TRF), which models the subcortical auditory pathway as a linear system, where a nonlinearly processed stimulus is taken as the input (i.e., regressor), the electroencephalogram (EEG) data as the output, and the ABR as the impulse response deconvolved from the recorded EEG and the regressor. In this study, we analyzed EEG recordings from subjects listening to both unaltered natural speech and synthesized “peaky speech.” We compared the derived ABR TRFs using three regressors: the half-wave rectified stimulus (HWR) from Maddox and Lee (2018), the glottal pulse train (GP) from Polonenko and Maddox (2021), and the auditory nerve modeled response (ANM; Zilany et al. (2014); (2009)) used in Shan et al. (2024). Our evaluation focused on the signal-to-noise ratio, prediction accuracy, efficiency, and practicality of applying each regressor in both unaltered and peaky speech. The results indicate that the ANM regressor with peaky speech provides the best performance, with the ANM for unaltered speech and the GP regressor for peaky speech close behind, whereas the HWR regressor demonstrated relatively poorer performance. There are, thus, multiple stimulus and analysis tools that can provide high-quality subcortical TRFs, with the choices for which to use dictated by experimental needs. The findings in this study will guide future research and clinical use in selecting the most appropriate paradigm for ABR derivation from continuous, naturalistic speech.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41598-023-50438-0
