Functional characterization of human Heschl's gyrus in response to natural speech.
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ABSTRACT:
SUBMITTER: Khalighinejad B
PROVIDER: S-EPMC8608271 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundSchizophrenia is a heterogeneous disorder that may consist of multiple etiologies and disease processes. Auditory hallucinations (AH), which are common and often disabling, represent a narrower and more basic dimension of psychosis than schizophrenia. Previous studies suggest that abnormal primary auditory cortex activity is associated with AH pathogenesis. We thus investigated functional connectivity, using a seed in primary auditory cortex, in schizophrenia patients with and without AH and healthy controls, to examine neural circuit abnormalities associated more specifically with AH than the myriad other symptoms that comprise schizophrenia.MethodsUsing resting-state fMRI (rsfMRI), we investigated functional connectivity of the primary auditory cortex, located on Heschl's gyrus, in schizophrenia spectrum patients with AH. Participants were patients with schizophrenia, schizoaffective disorder, or schizophreniform disorder with lifetime AH (n=27); patients with the same diagnoses but no lifetime AH (n=14); and healthy controls (n=28).ResultsPatients with AH vulnerability showed increased left Heschl's gyrus functional connectivity with left frontoparietal regions and decreased functional connectivity with right hippocampal formation and mediodorsal thalamus compared to patients without lifetime AH. Furthermore, among AH patients, left Heschl's gyrus functional connectivity covaried positively with AH severity in left inferior frontal gyrus (Broca's area), left lateral STG, right pre- and postcentral gyri, cingulate cortex, and orbitofrontal cortex. There were no differences between patients with and without lifetime AH in right Heschl's gyrus seeded functional connectivity.ConclusionsAbnormal interactions between left Heschl's gyrus and regions involved in speech/language, memory, and the monitoring of self-generated events may contribute to AH vulnerability.
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Project description:The way in which normal variations in human neuroanatomy relate to brain function remains largely uninvestigated. This study addresses the question by relating anatomical measurements of Heschl's gyrus (HG), the structure containing human primary auditory cortex, to how this region processes temporal and spectral acoustic information. In this study, subjects' right and left HG were identified and manually indicated on anatomical magnetic resonance imaging scans. Volumes of gray matter, white matter, and total gyrus were recorded, and asymmetry indices were calculated. Additionally, cortical auditory activity in response to noise stimuli varying orthogonally in temporal and spectral dimensions was assessed and related to the volumetric measurements. A high degree of anatomical variability was seen, consistent with other reports in the literature. The auditory cortical responses showed the expected leftward lateralization to varying rates of stimulus change and rightward lateralization of increasing spectral information. An explicit link between auditory structure and function is then established, in which anatomical variability of auditory cortex is shown to relate to individual differences in the way that cortex processes acoustic information. Specifically, larger volumes of left HG were associated with larger extents of rate-related cortex on the left, and larger volumes of right HG related to larger extents of spectral-related cortex on the right. This finding is discussed in relation to known microanatomical asymmetries of HG, including increased myelination of its fibers, and implications for language learning are considered.
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Project description:Auditory cortex volume and shape differences have been observed in the context of phonetic learning, musicianship and dyslexia. Heschl's gyrus, which includes primary auditory cortex, displays large anatomical variability across individuals and hemispheres. Given this variability, manual labelling is the gold standard for segmenting HG, but is time consuming and error prone. Our novel toolbox, called 'Toolbox for the Automated Segmentation of HG' or TASH, automatically segments HG in brain structural MRI data, and extracts measures including its volume, surface area and cortical thickness. TASH builds upon FreeSurfer, which provides an initial segmentation of auditory regions, and implements further steps to perform finer auditory cortex delineation. We validate TASH by showing significant relationships between HG volumes obtained using manual labelling and using TASH, in three independent datasets acquired on different scanners and field strengths, and by showing good qualitative segmentation. We also present two applications of TASH, demonstrating replication and extension of previously published findings of relationships between HG volumes and (a) phonetic learning, and (b) musicianship. In sum, TASH effectively segments HG in a fully automated and reproducible manner, opening up a wide range of applications in the domains of expertise, disease, genetics and brain plasticity.
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Project description:The capacity of auditory cortex on Heschl's gyrus (HG) to encode repetitive transients was studied in human patients undergoing surgical evaluation for medically intractable epilepsy. Multicontact depth electrodes were chronically implanted in gray matter of HG. Bilaterally presented stimuli were click trains varying in rate from 4 to 200 Hz. Averaged evoked potentials (AEPs) and event-related band power (ERBP), computed from responses at each of 14 recording sites, identified two auditory fields. A core field, which occupies posteromedial HG, was characterized by a robust polyphasic AEP on which could be superimposed a frequency following response (FFR). The FFR was prominent at click rates below approximately 50 Hz, decreased rapidly as click rate was increased, but could reliably be detected at click rates as high as 200 Hz. These data are strikingly similar to those obtained by others in the monkey under essentially the same stimulus conditions, indicating that mechanisms underlying temporal processing in the auditory core may be highly conserved across primate species. ERBP, which reflects increases or decreases of both phase-locked and non-phase-locked power within given frequency bands, showed stimulus-related increases in gamma band frequencies as high as 250 Hz. The AEPs recorded in a belt field anterolateral to the core were typically of low amplitude, showing little or no evidence of short-latency waves or an FFR, even at the lowest click rates used. The non-phase-locked component of the response extracted from the ERBP showed a robust, long-latency response occurring here in response to the highest click rates in the series.
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Project description:A number of brain regions have been implicated in articulation, but their precise computations remain debated. Using functional magnetic resonance imaging, we examine the degree of functional specificity of articulation-responsive brain regions to constrain hypotheses about their contributions to speech production. We find that articulation-responsive regions (1) are sensitive to articulatory complexity, but (2) are largely nonoverlapping with nearby domain-general regions that support diverse goal-directed behaviors. Furthermore, premotor articulation regions show selectivity for speech production over some related tasks (respiration control), but not others (nonspeech oral-motor [NSO] movements). This overlap between speech and nonspeech movements concords with electrocorticographic evidence that these regions encode articulators and their states, and with patient evidence whereby articulatory deficits are often accompanied by oral-motor deficits. In contrast, the superior temporal regions show strong selectivity for articulation relative to nonspeech movements, suggesting that these regions play a specific role in speech planning/production. Finally, articulation-responsive portions of posterior inferior frontal gyrus show some selectivity for articulation, in line with the hypothesis that this region prepares an articulatory code that is passed to the premotor cortex. Taken together, these results inform the architecture of the human articulation system.
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Project description:The human auditory cortex around Heschl's gyrus (HG) exhibits diverging patterns across individuals owing to the heterogeneity of its substructures. In this study, we investigated the subregions of the human auditory cortex using data-driven machine-learning techniques at the individual level and assessed their structural and functional profiles. We studied an openly accessible large dataset of the Human Connectome Project and identified the subregions of the HG in humans using data-driven clustering techniques with individually calculated imaging features of cortical folding and structural connectivity information obtained via diffusion magnetic resonance imaging tractography. We characterized the structural and functional profiles of each HG subregion according to the cortical morphology, microstructure, and functional connectivity at rest. We found three subregions. The first subregion (HG1) occupied the central portion of HG, the second subregion (HG2) occupied the medial-posterior-superior part of HG, and the third subregion (HG3) occupied the lateral-anterior-inferior part of HG. The HG3 exhibited strong structural and functional connectivity to the association and paralimbic areas, and the HG1 exhibited a higher myelin density and larger cortical thickness than other subregions. A functional gradient analysis revealed a gradual axis expanding from the HG2 to the HG3. Our findings clarify the individually varying structural and functional organization of human HG subregions and provide insights into the substructures of the human auditory cortex.
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Project description:Speech perception requires the rapid and effortless extraction of meaningful phonetic information from a highly variable acoustic signal. A powerful example of this phenomenon is categorical speech perception, in which a continuum of acoustically varying sounds is transformed into perceptually distinct phoneme categories. We found that the neural representation of speech sounds is categorically organized in the human posterior superior temporal gyrus. Using intracranial high-density cortical surface arrays, we found that listening to synthesized speech stimuli varying in small and acoustically equal steps evoked distinct and invariant cortical population response patterns that were organized by their sensitivities to critical acoustic features. Phonetic category boundaries were similar between neurometric and psychometric functions. Although speech-sound responses were distributed, spatially discrete cortical loci were found to underlie specific phonetic discrimination. Our results provide direct evidence for acoustic-to-higher order phonetic level encoding of speech sounds in human language receptive cortex.
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Project description:How the brain extracts words from auditory signals is an unanswered question. We recorded approximately 150 single and multi-units from the left anterior superior temporal gyrus of a patient during multiple auditory experiments. Against low background activity, 45% of units robustly fired to particular spoken words with little or no response to pure tones, noise-vocoded speech, or environmental sounds. Many units were tuned to complex but specific sets of phonemes, which were influenced by local context but invariant to speaker, and suppressed during self-produced speech. The firing of several units to specific visual letters was correlated with their response to the corresponding auditory phonemes, providing the first direct neural evidence for phonological recoding during reading. Maximal decoding of individual phonemes and words identities was attained using firing rates from approximately 5 neurons within 200 ms after word onset. Thus, neurons in human superior temporal gyrus use sparse spatially organized population encoding of complex acoustic-phonetic features to help recognize auditory and visual words.
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Project description:Heightened auditory sensitivity and atypical auditory processing are common in autism. Functional studies suggest abnormal neural response and hemispheric activation to auditory stimuli, yet the neurodevelopment underlying atypical auditory function in autism is unknown. In this study, we model longitudinal volumetric growth of Heschl's gyrus gray matter and white matter during childhood and adolescence in 40 individuals with autism and 17 typically developing participants. Up to three time points of magnetic resonance imaging data, collected on average every 2.5 years, were examined from individuals 3-12 years of age at the time of their first scan. Consistent with previous cross-sectional studies, no group differences were found in Heschl's gyrus gray matter volume or asymmetry. However, reduced longitudinal gray matter volumetric growth was found in the right Heschl's gyrus in autism. Reduced longitudinal white matter growth in the left hemisphere was found in the right-handed autism participants. Atypical Heschl's gyrus white matter volumetric growth was found bilaterally in the autism individuals with a history of delayed onset of spoken language. Heightened auditory sensitivity, obtained from the Sensory Profile, was associated with reduced volumetric gray matter growth in the right hemisphere. Our longitudinal analyses revealed dynamic gray and white matter changes in Heschl's gyrus throughout childhood and adolescence in both typical development and autism.
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Project description:Deficit syndrome schizophrenia is a characteristic subtype defined by persistent negative symptoms and poor functional outcomes; however, the biological mechanisms underlying this specific subtype have not yet been elucidated in detail. The present magnetic resonance imaging study examined the prevalence of duplicated Heschl's gyrus (HG), a potential neurodevelopmental marker, in schizophrenia patients with (N = 38) and without (N = 37) the deficit syndrome. The prevalence of the HG duplication pattern bilaterally was higher in the whole schizophrenia group than in 59 matched healthy controls. Furthermore, the prevalence of right HG duplication was significantly higher in the deficit schizophrenia group than in the non-deficit schizophrenia group. The HG pattern in schizophrenia was not associated with clinical variables, including illness duration, medication, and symptom severity, while right HG duplication correlated with higher scores for Proxy for the Deficit Syndrome. The present results suggest that the prominent neurodevelopmental pathology associated with gyral formation of HG may contribute to enduring negative symptomatology in schizophrenia.
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