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High-density intracranial recordings reveal a distinct site in anterior dorsal precentral cortex that tracks perceived speech.

ABSTRACT: Various brain regions are implicated in speech processing, and the specific function of some of them is better understood than others. In particular, involvement of the dorsal precentral cortex (dPCC) in speech perception remains debated, and attribution of the function of this region is more or less restricted to motor processing. In this study, we investigated high-density intracranial responses to speech fragments of a feature film, aiming to determine whether dPCC is engaged in perception of continuous speech. Our findings show that dPCC exhibited preference to speech over other tested sounds. Moreover, the identified area was involved in tracking of speech auditory properties including speech spectral envelope, its rhythmic phrasal pattern and pitch contour. DPCC also showed the ability to filter out noise from the perceived speech. Comparing these results to data from motor experiments showed that the identified region had a distinct location in dPCC, anterior to the hand motor area and superior to the mouth articulator region. The present findings uncovered with high-density intracranial recordings help elucidate the functional specialization of PCC and demonstrate the unique role of its anterior dorsal region in continuous speech perception.

SUBMITTER: Berezutskaya J

PROVIDER: S-EPMC7555065 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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High-density intracranial recordings reveal a distinct site in anterior dorsal precentral cortex that tracks perceived speech.

Berezutskaya Julia J Baratin Clarissa C Freudenburg Zachary V ZV Ramsey Nicolas F NF

Human brain mapping 20200803 16

Various brain regions are implicated in speech processing, and the specific function of some of them is better understood than others. In particular, involvement of the dorsal precentral cortex (dPCC) in speech perception remains debated, and attribution of the function of this region is more or less restricted to motor processing. In this study, we investigated high-density intracranial responses to speech fragments of a feature film, aiming to determine whether dPCC is engaged in perception of ...[more]

PMID: 32744403

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Project description:IntroductionCochlear implants (CIs) are the treatment of choice for severe to profound hearing loss. Variability in CI outcomes remains despite advances in technology and is attributed in part to differences in cortical processing. Studying these differences in CI users is technically challenging. Spectrally degraded stimuli presented to normal-hearing individuals approximate input to the central auditory system in CI users. This study used intracranial electroencephalography (iEEG) to investigate cortical processing of spectrally degraded speech.MethodsParticipants were adult neurosurgical epilepsy patients. Stimuli were utterances /aba/ and /ada/, spectrally degraded using a noise vocoder (1-4 bands) or presented without vocoding. The stimuli were presented in a two-alternative forced choice task. Cortical activity was recorded using depth and subdural iEEG electrodes. Electrode coverage included auditory core in posteromedial Heschl's gyrus (HGPM), superior temporal gyrus (STG), ventral and dorsal auditory-related areas, and prefrontal and sensorimotor cortex. Analysis focused on high gamma (70-150 Hz) power augmentation and alpha (8-14 Hz) suppression.ResultsChance task performance occurred with 1-2 spectral bands and was near-ceiling for clear stimuli. Performance was variable with 3-4 bands, permitting identification of good and poor performers. There was no relationship between task performance and participants demographic, audiometric, neuropsychological, or clinical profiles. Several response patterns were identified based on magnitude and differences between stimulus conditions. HGPM responded strongly to all stimuli. A preference for clear speech emerged within non-core auditory cortex. Good performers typically had strong responses to all stimuli along the dorsal stream, including posterior STG, supramarginal, and precentral gyrus; a minority of sites in STG and supramarginal gyrus had a preference for vocoded stimuli. In poor performers, responses were typically restricted to clear speech. Alpha suppression was more pronounced in good performers. In contrast, poor performers exhibited a greater involvement of posterior middle temporal gyrus when listening to clear speech.DiscussionResponses to noise-vocoded speech provide insights into potential factors underlying CI outcome variability. The results emphasize differences in the balance of neural processing along the dorsal and ventral stream between good and poor performers, identify specific cortical regions that may have diagnostic and prognostic utility, and suggest potential targets for neuromodulation-based CI rehabilitation strategies.

Project description:Cigarette smoking has a major impact on global health and morbidity, and positron emission tomographic research has provided evidence for reduced inflammation in the human brain associated with cigarette smoking. Given the consequences of inflammatory dysfunction for health, the question of whether cigarette smoking affects neuroinflammation warrants further investigation. The goal of this project therefore was to validate and extend evidence of hypoinflammation related to smoking, and to examine the potential contribution of inflammation to clinical features of smoking. Using magnetic resonance spectroscopy, we measured levels of neurometabolites that are putative neuroinflammatory markers. N-acetyl compounds (N-acetylaspartate + N-acetylaspartylglutamate), glutamate, creatine, choline-compounds (phosphocholine + glycerophosphocholine), and myo-inositol, have all been linked to neuroinflammation, but they have not been examined as such with respect to smoking. We tested whether people who smoke cigarettes have brain levels of these metabolites consistent with decreased neuroinflammation, and whether clinical features of smoking are associated with levels of these metabolites. The dorsal anterior cingulate cortex was chosen as the region-of-interest because of previous evidence linking it to smoking and related states. Fifty-four adults who smoked daily maintained overnight smoking abstinence before testing and were compared with 37 nonsmoking participants. Among the smoking participants, we tested for associations of metabolite levels with tobacco dependence, smoking history, craving, and withdrawal. Levels of N-acetyl compounds and glutamate were higher, whereas levels of creatine and choline compounds were lower in the smoking group as compared with the nonsmoking group. In the smoking group, glutamate and creatine levels correlated negatively with tobacco dependence, and creatine correlated negatively with lifetime smoking, but none of the metabolite levels correlated with craving or withdrawal. The findings indicate a link between smoking and a hypoinflammatory state in the brain, specifically in the dorsal anterior cingulate cortex. Smoking may thereby increase vulnerability to infection and brain injury.

Project description:ObjectiveTo evaluate the potential of intracortical electrode array signals for brain-computer interfaces (BCIs) to restore lost speech, we measured the performance of decoders trained to discriminate a comprehensive basis set of 39 English phonemes and to synthesize speech sounds via a neural pattern matching method. We decoded neural correlates of spoken-out-loud words in the 'hand knob' area of precentral gyrus, a step toward the eventual goal of decoding attempted speech from ventral speech areas in patients who are unable to speak.ApproachNeural and audio data were recorded while two BrainGate2 pilot clinical trial participants, each with two chronically-implanted 96-electrode arrays, spoke 420 different words that broadly sampled English phonemes. Phoneme onsets were identified from audio recordings, and their identities were then classified from neural features consisting of each electrode's binned action potential counts or high-frequency local field potential power. Speech synthesis was performed using the 'Brain-to-Speech' pattern matching method. We also examined two potential confounds specific to decoding overt speech: acoustic contamination of neural signals and systematic differences in labeling different phonemes' onset times.Main resultsA linear decoder achieved up to 29.3% classification accuracy (chance = 6%) across 39 phonemes, while an RNN classifier achieved 33.9% accuracy. Parameter sweeps indicated that performance did not saturate when adding more electrodes or more training data, and that accuracy improved when utilizing time-varying structure in the data. Microphonic contamination and phoneme onset differences modestly increased decoding accuracy, but could be mitigated by acoustic artifact subtraction and using a neural speech onset marker, respectively. Speech synthesis achieved r = 0.523 correlation between true and reconstructed audio.SignificanceThe ability to decode speech using intracortical electrode array signals from a nontraditional speech area suggests that placing electrode arrays in ventral speech areas is a promising direction for speech BCIs.

Dataset Information

High-density intracranial recordings reveal a distinct site in anterior dorsal precentral cortex that tracks perceived speech.

Publications

High-density intracranial recordings reveal a distinct site in anterior dorsal precentral cortex that tracks perceived speech.

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