Hierarchical Organization of Human Auditory Cortex: Evidence from Acoustic Invariance in the Response to Intelligible Speech

Okada, Kayoko; Rong, Feng; Venezia, Jon; Matchin, William; Hsieh, I‐Hui; Saberi, Kourosh; Serences, John T.; Hickok, Gregory

doi:10.1093/cercor/bhp318

Cited by 242 publications

(265 citation statements)

References 47 publications

Supporting

Mentioning

215

Contrasting

Order By: Relevance

“…In line with our predictions, we found that short timescale areas, including primary auditory cortex, showed only small neural differences in response to local word changes. This finding is consistent with observations that these early auditory areas process transient and rapidly changing sensory input (23,24), such that brief local alternations in the sound structure will only induce brief and local alternations in the neural responses across the two stories. However, neural differences in response across the two groups gradually increased along the processing timescale hierarchy, with the largest neural distance in areas with a long TRW, including TPJ, angular gyrus, posterior cingulate cortex, and dorsomedial prefrontal cortex.…”

Section: Discussionsupporting

confidence: 91%

Amplification of local changes along the timescale processing hierarchy

Yeshurun

Nguyen

Hasson

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Small changes in word choice can lead to dramatically different interpretations of narratives. How does the brain accumulate and integrate such local changes to construct unique neural representations for different stories? In this study, we created two distinct narratives by changing only a few words in each sentence (e.g., "he" to "she" or "sobbing" to "laughing") while preserving the grammatical structure across stories. We then measured changes in neural responses between the two stories. We found that differences in neural responses between the two stories gradually increased along the hierarchy of processing timescales. For areas with short integration windows, such as early auditory cortex, the differences in neural responses between the two stories were relatively small. In contrast, in areas with the longest integration windows at the top of the hierarchy, such as the precuneus, temporal parietal junction, and medial frontal cortices, there were large differences in neural responses between stories. Furthermore, this gradual increase in neural differences between the stories was highly correlated with an area's ability to integrate information over time. Amplification of neural differences did not occur when changes in words did not alter the interpretation of the story (e.g., sobbing to "crying"). Our results demonstrate how subtle differences in words are gradually accumulated and amplified along the cortical hierarchy as the brain constructs a narrative over time.timescale | amplification | fMRI | narrative | hierarchy S tories unfold over many minutes and are organized into temporarily nested structures: Paragraphs are made of sentences, which are made of words, which are made of phonemes. Understanding a story therefore requires processing the story at multiple timescales, starting with the integration of phonemes to words within a relatively short temporal window, to the integration of words to sentences across a longer temporal window of a few seconds, and up to the integration of sentences and paragraphs into a coherent narrative over many minutes. It was recently suggested that the temporally nested structure of language is processed hierarchically along the cortical surface (1-4). A consequence of the hierarchical structure of language is that small changes in word choice can give rise to large differences in sentence and overall narrative interpretation. Here, we propose that local momentary changes in linguistic input in the context of a narrative (e.g., "he" to "she" or "sobbing" to "laughing") are accumulated and amplified during the processing of linguistic content across the cortex. Specifically, we hypothesize that as areas in the brain increase in their ability to integrate information over time (e.g., processing "word" level content vs. "sentence" or "narrative" level content), the neural response to small word changes will become increasingly divergent.Previously, we defined a temporal receptive window (TRW) as the length of time during which prior information from an ongoing stimulu...

show abstract

Section: Discussionsupporting

confidence: 91%

Amplification of local changes along the timescale processing hierarchy

Yeshurun

Nguyen

Hasson

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…As shown in Figure 5, most of the above areas modulated by intelligibility overlapped with those showing a collapse at the shortest duration of sentence presentation. Thus, these two independent criteria converge to suggest that activation in left superior temporal and inferior frontal regions drops to a nearzero level when sentences cease to be intelligible, in agreement with previous findings (Davis and Johnsrude, 2003;Friederici et al, 2010;Okada et al, 2010). An exception was the temporal parietal junction, which was modulated by intelligibility but did not show a collapse at short sentence duration.…”

Section: Activations Linked To Intelligibilitysupporting

confidence: 91%

“…In higher-order language areas, indeed, previous publications (Davis and Johnsrude, 2003;Friederici et al, 2010;Okada et al, 2010) led us to expect the fMRI signal to reflect the intelligibility associated with each compression condition rather than the physical compression rate itself. Indeed, many regions showed a nonlinear profile of activation with duration ( Fig.…”

Section: Regions With a Collapse At The Shortest Duration Of Presentamentioning

confidence: 90%

A Temporal Bottleneck in the Language Comprehension Network

Vagharchakian¹,

Dehaene‐Lambertz²,

Pallier³

et al. 2012

Journal of Neuroscience

101

View full text Add to dashboard Cite

Humans can understand spoken or written sentences presented at extremely fast rates of ϳ400 wpm, far exceeding the normal speech rate (ϳ150 wpm). How does the brain cope with speeded language? And what processing bottlenecks eventually make language incomprehensible above a certain presentation rate? We used time-resolved fMRI to probe the brain responses to spoken and written sentences presented at five compression rates, ranging from intelligible (60 -100% of the natural duration) to challenging (40%) and unintelligible (20%). The results show that cortical areas differ sharply in their activation speed and amplitude. In modality-specific sensory areas, activation varies linearly with stimulus duration. However, a large modality-independent left-hemispheric language network, including the inferior frontal gyrus (pars orbitalis and triangularis) and the superior temporal sulcus, shows a remarkably time-invariant response, followed by a sudden collapse for unintelligible stimuli. Finally, linear and nonlinear responses, reflecting a greater effort as compression increases, are seen at various prefrontal and parietal sites. We show that these profiles fit with a simple model according to which the higher stages of language processing operate at a fixed speed and thus impose a temporal bottleneck on sentence comprehension. At presentation rates faster than this internal processing speed, incoming words must be buffered, and intelligibility vanishes when buffer storage and retrieval operations are saturated. Based on their temporal and amplitude profiles, buffer regions can be identified with the left inferior frontal/anterior insula, precentral cortex, and mesial frontal cortex.

show abstract

“…For example, extraction of relational properties across variations consequent to coarticulation (e.g., locus equations, Sussman et al, 1991Sussman et al, , 1998 or anatomy (scaling of formant frequencies across changes in vocal tract length across talkers, Kluender et al, 2011) are the most direct speech analogs to non-isomorphism demonstrated here. In related studies employing fMRI, Okada et al (2010) report that responses in bilateral posterior superior temporal sulcus were sensitive to phonemic variability (intelligibility) of speech sounds, but not to acoustic variability. These and other examples support the notion that high-level auditory processing captures abstract characteristics of complex stimuli.…”

Section: Discussionmentioning

confidence: 99%

Non-isomorphism in efficient coding of complex sound properties

Stilp

Kluender

2011

The Journal of the Acoustical Society of America

View full text Add to dashboard Cite

To the extent that sensorineural systems are efficient, stimulus redundancy should be captured in ways that optimize information transmission. Consistent with this principle, neural representations of sounds have been proposed to become “non-isomorphic,” increasingly abstract and decreasingly resembling the original (redundant) input. Here, non-isomorphism is tested in perceptual learning using AXB discrimination of novel sounds with two highly correlated complex acoustic properties and a randomly varying third dimension. Discrimination of sounds obeying the correlation became superior to that of sounds violating it despite widely varying physical acoustic properties, suggesting non-isomorphic representation of stimulus redundancy.

show abstract

Hierarchical Organization of Human Auditory Cortex: Evidence from Acoustic Invariance in the Response to Intelligible Speech

Cited by 242 publications

References 47 publications

Amplification of local changes along the timescale processing hierarchy

Amplification of local changes along the timescale processing hierarchy

A Temporal Bottleneck in the Language Comprehension Network

Non-isomorphism in efficient coding of complex sound properties

Contact Info

Product

Resources

About