How the auditory system encodes speech sounds is not well understood, and animal models have a lot to offer in investigating such questions. This study evaluated the representations of a variety of natural and synthetic sounds in both ferrets and humans, and reported that humans differed from ferrets in the manner in which speech and music were represented, despite controlling for the spectrotemporal content of the sounds. This work makes an important contribution to our understanding of how the coding of such sounds differs across species.
more »
« less
Distinct higher-order representations of natural sounds in human and ferret auditory cortex
Little is known about how neural representations of natural sounds differ across species. For example, speech and music play a unique role in human hearing, yet it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional ultrasound imaging, we measured responses in ferrets to a set of natural and spectrotemporally matched synthetic sounds previously tested in humans. Ferrets showed similar lower-level frequency and modulation tuning to that observed in humans. But while humans showed substantially larger responses to natural vs. synthetic speech and music in non-primary regions, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary auditory cortex, even when tested with ferret vocalizations. This finding reveals that auditory representations in humans and ferrets diverge sharply at late stages of cortical processing, potentially driven by higher-order processing demands in speech and music.
more »
« less
- Award ID(s):
- 2020624
- NSF-PAR ID:
- 10376895
- Date Published:
- Journal Name:
- eLife
- Volume:
- 10
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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.more » « less
-
more » « less
Neural speech tracking has advanced our understanding of how our brains rapidly map an acoustic speech signal onto linguistic representations and ultimately meaning. It remains unclear, however, how speech intelligibility is related to the corresponding neural responses. Many studies addressing this question vary the level of intelligibility by manipulating the acoustic waveform, but this makes it difficult to cleanly disentangle the effects of intelligibility from underlying acoustical confounds. Here, using magnetoencephalography recordings, we study neural measures of speech intelligibility by manipulating intelligibility while keeping the acoustics strictly unchanged. Acoustically identical degraded speech stimuli (three-band noise-vocoded, ~20 s duration) are presented twice, but the second presentation is preceded by the original (nondegraded) version of the speech. This intermediate priming, which generates a “pop-out” percept, substantially improves the intelligibility of the second degraded speech passage. We investigate how intelligibility and acoustical structure affect acoustic and linguistic neural representations using multivariate temporal response functions (mTRFs). As expected, behavioral results confirm that perceived speech clarity is improved by priming. mTRFs analysis reveals that auditory (speech envelope and envelope onset) neural representations are not affected by priming but only by the acoustics of the stimuli (bottom–up driven). Critically, our findings suggest that segmentation of sounds into words emerges with better speech intelligibility, and most strongly at the later (~400 ms latency) word processing stage, in prefrontal cortex, in line with engagement of top–down mechanisms associated with priming. Taken together, our results show that word representations may provide some objective measures of speech comprehension.
-
more » « less
Abstract Speech processing often occurs amid competing inputs from other modalities, for example, listening to the radio while driving. We examined the extent to which dividing attention between auditory and visual modalities (bimodal divided attention) impacts neural processing of natural continuous speech from acoustic to linguistic levels of representation. We recorded electroencephalographic (EEG) responses when human participants performed a challenging primary visual task, imposing low or high cognitive load while listening to audiobook stories as a secondary task. The two dual-task conditions were contrasted with an auditory single-task condition in which participants attended to stories while ignoring visual stimuli. Behaviorally, the high load dual-task condition was associated with lower speech comprehension accuracy relative to the other two conditions. We fitted multivariate temporal response function encoding models to predict EEG responses from acoustic and linguistic speech features at different representation levels, including auditory spectrograms and information-theoretic models of sublexical-, word-form-, and sentence-level representations. Neural tracking of most acoustic and linguistic features remained unchanged with increasing dual-task load, despite unambiguous behavioral and neural evidence of the high load dual-task condition being more demanding. Compared to the auditory single-task condition, dual-task conditions selectively reduced neural tracking of only some acoustic and linguistic features, mainly at latencies >200 ms, while earlier latencies were surprisingly unaffected. These findings indicate that behavioral effects of bimodal divided attention on continuous speech processing occur not because of impaired early sensory representations but likely at later cognitive processing stages. Crossmodal attention-related mechanisms may not be uniform across different speech processing levels.
-
more » « less
It has been postulated that the brain is organized by “metamodal,” sensory-independent cortical modules capable of performing tasks (e.g., word recognition) in both “standard” and novel sensory modalities. Still, this theory has primarily been tested in sensory-deprived individuals, with mixed evidence in neurotypical subjects, thereby limiting its support as a general principle of brain organization. Critically, current theories of metamodal processing do not specify requirements for successful metamodal processing at the level of neural representations. Specification at this level may be particularly important in neurotypical individuals, where novel sensory modalities must interface with existing representations for the standard sense. Here we hypothesized that effective metamodal engagement of a cortical area requires congruence between stimulus representations in the standard and novel sensory modalities in that region. To test this, we first used fMRI to identify bilateral auditory speech representations. We then trained 20 human participants (12 female) to recognize vibrotactile versions of auditory words using one of two auditory-to-vibrotactile algorithms. The vocoded algorithm attempted to match the encoding scheme of auditory speech while the token-based algorithm did not. Crucially, using fMRI, we found that only in the vocoded group did trained-vibrotactile stimuli recruit speech representations in the superior temporal gyrus and lead to increased coupling between them and somatosensory areas. Our results advance our understanding of brain organization by providing new insight into unlocking the metamodal potential of the brain, thereby benefitting the design of novel sensory substitution devices that aim to tap into existing processing streams in the brain.
SIGNIFICANCE STATEMENT It has been proposed that the brain is organized by “metamodal,” sensory-independent modules specialized for performing certain tasks. This idea has inspired therapeutic applications, such as sensory substitution devices, for example, enabling blind individuals “to see” by transforming visual input into soundscapes. Yet, other studies have failed to demonstrate metamodal engagement. Here, we tested the hypothesis that metamodal engagement in neurotypical individuals requires matching the encoding schemes between stimuli from the novel and standard sensory modalities. We trained two groups of subjects to recognize words generated by one of two auditory-to-vibrotactile transformations. Critically, only vibrotactile stimuli that were matched to the neural encoding of auditory speech engaged auditory speech areas after training. This suggests that matching encoding schemes is critical to unlocking the brain's metamodal potential.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.65566
