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Brang, D.

Publications and source records attributed to Brang, D..

12 recordsLinked to original sources

Human iEEG recordings during audiovisual speech violations support and extend predictive routing models

Rather than constantly reconstructing the world solely through sensory input, predictive processing theories posit that the brain utilizes predictions maintained as internal representations to guide sensory processing. An emerging model, predictive routing, proposes that an interplay between neuronal gamma (40-150 Hz) and alpha-beta (10-30 Hz) rhythms implements a dynamic mechanism for predictive processing. Namely, predictions enhance alpha-beta oscillations that suppress gamma activity during the processing of predicted inputs. While this model is supported by animal studies, its validity has not been fully explored within the human brain. The present study addresses this by leveraging human intracranial EEG (iEEG) recordings across superior temporal and prefrontal/premotor areas of seven presurgical epilepsy patients during an audiovisual speech paradigm. We calculated iEEG power in the theta, alpha-beta, and high gamma bands during simple auditory deviance, multisensory integration, and a condition where an incongruent visual cue (lip movements) clashed with an auditory stimulus (a syllable), creating audiovisual incongruence that can elicit the McGurk illusion. Results revealed increased high-gamma and decreased alpha-beta power in the superior temporal cortex in response to auditory deviance and the McGurk condition, while frontal areas, despite reflecting a similar decrease in alpha-beta power, did not present this high gamma prediction error signal. Instead, the theta band revealed a strong prediction error signal in the McGurk condition, consistent with theories on the role of theta in reorganizing cortical networks. These results both support and extend existing predictive routing models for human-specific forms of predictive processing.

neuroscience↗

Visual speech enhances phoneme separability in human superior temporal gyrus

Visual speech, such as lipreading, facilitates spoken word recognition, but the neural mechanisms underlying audiovisual speech perception remain poorly understood. Visual cues may disambiguate fine-grained articulatory features during early perceptual stages or instead integrate with speech at more categorical, phoneme-level stages. To test how speech representations are modulated by visual input, we analyzed intracranial electroencephalography (iEEG) signals recorded from 12 epilepsy patients performing an audiovisual speech perception task. Participants perceived 16 monosyllabic words presented in auditory-only, visual-only, or congruent audiovisual formats. Words were constructed from four onset consonants (/b/, /g/, /m/, /n/) and four rimes (vowel nucleus and any coda consonants). We examined event-related potentials (ERP) in superior temporal gyrus (STG) and trained support vector machine (SVM) classifiers to decode word identity from neural activity at individual electrodes. Discrete and continuous confusion matrices captured complementary changes in classification accuracy and normalized inverse classification loss, a continuous proxy for classifier confidence. Decoding performance was hierarchically evaluated at the word, phoneme, and phonetic feature levels to determine the representations affected by visual speech. Congruent audiovisual speech increased classifier confidence for phoneme-level representations and improved decoding accuracy at both the word and phoneme level, without corresponding effects on phonetic features. Time-resolved analyses further revealed earlier successful decoding for audiovisual than auditory-only speech, with audiovisual enhancement primarily observed for onset consonants rather than rimes. Together, these findings suggest that visual speech sharpens primarily categorical phoneme representations in STG, with accelerated speech processing and improved word recognition emerging as downstream consequences of phoneme-level enhancement.

neuroscience↗

Electrocorticographic Detection of Speech Networks in Glioma-infiltrated Cortex

Direct cortical stimulation (DCS) is the clinical gold standard for identifying functional cortex in the human brain, which is essential for the safe removal of brain lesions. Defining the electro-physiological properties of DCS- positive cortical regions may facilitate the identification of critical language regions, thereby permitting safe glioma resections in communities without access. Leveraging a multicenter electrophysiologic dataset of DCS- positive language regions spatially matched with subdural arrays, we analyzed regions identified as functionally critical (DCS+) versus functionally non-critical (DCS-) during intraoperative language mapping. In IDH-mutant gliomas, DCS+ regions exhibited significantly greater speech-related neural activity and enhanced encoding and decoding of linguistic and semantic features. We demonstrate that resting-state classifiers distinguish DCS+ from DCS- regions in IDH-mutant tumors. Task-based and resting-state electrophysiologic distinctions were pathology-specific and not present in IDH-wildtype glioblastomas. These findings may accelerate DCS mapping by guiding surgeons to priority regions, improving efficiency, and patient outcomes.

neuroscience↗

Aperiodic neural dynamics define a novel signature of glioma-induced excitation-inhibition dysregulation

Diffuse gliomas remodel neuronal circuits with prognostic and therapeutic significance for patients. Electrophysiologic measures of cortical excitability hold promise for monitoring disease progression and evaluating therapeutic responses. The power law exponent (aperiodic slope) reflects the balance between excitatory and inhibitory activity within neuronal networks, a critical aspect of normal brain function often disrupted in neurological conditions. Despite its potential, the significance of the aperiodic slope in glioma-infiltrated tissue and its underlying cellular processes has not been fully investigated. Here, we integrate multi-modal electrophysiological analysis with transcriptomic profiling to analyze the aperiodic slope in both normal and glioma-infiltrated cortex. We determine that glioma infiltration induces a flattening of the aperiodic slope, indicating a shift toward excitation dominance that varies according to tumor subtype and correlates with impairments in semantic naming. Single-nucleus RNA sequencing revealed that cortical regions with flat aperiodic slope exhibit transcriptional programs enriched in glutamatergic signaling, membrane depolarization, and excitatory synaptic transmission. The aperiodic slope responds to pharmacologically induced changes in cortical inhibition during propofol administration, a GABAA agonist. Our results establish the aperiodic slope as a robust biomarker of glioma-associated excitation-inhibition imbalance, with potential applications in tumor classification and treatment monitoring.

cancer biology↗

Electrical stimulation of the superior temporal gyrus evokes rapid responses in human visual cortex

Sounds elicit rapid responses in human visual cortex. Anatomical work in nonhuman primates suggests that these responses may be enabled by monosynaptic, corticocortical projections between auditory and visual areas. Such projections would not only provide routes for rapid modulation of visual processing in the sighted, but also avenues for cortical adaptation following vision loss. However, there is little available information on the presence and organization of such projections in humans. Here, we address this question by examining intracranial responses to direct electrical stimulation of the superior temporal gyrus (STG) in 23 patients (both male and female). Mid- and posterior-STG stimulation produced rapid responses in early visual cortex (18ms+), with a distribution that favored lateral occipital cortex and anterior calcarine regions near peripheral V1. Early visual cortex (V1/V2) responded most strongly to stimulation over mid-STG, whereas lateral occipital cortex (near V5/hMT+) exhibited the most robust response to posterior STG stimulation. These data demonstrate that communication from auditory to visual cortex can occur in humans at latencies that are compatible with corticocortical, potentially monosynaptic, transmission. Responses in visual cortex were organized in a manner similar to that of nonhuman primates, with preliminary evidence for an exception over the occipital pole. Overall, the results provide support for theories that human visual responses to sound are inherited, in part, from auditory cortex.

neuroscience↗

Evidence for a Causal Dissociation of the McGurk Effect and Congruent Audiovisual Speech Perception via TMS

Congruent visual speech improves speech perception accuracy, particularly in noisy environments. Conversely, mismatched visual speech can alter what is heard, leading to an illusory percept known as the McGurk effect. This illusion has been widely used to study audiovisual speech integration, illustrating that auditory and visual cues are combined in the brain to generate a single coherent percept. While prior transcranial magnetic stimulation (TMS) and neuroimaging studies have identified the left posterior superior temporal sulcus (pSTS) as a causal region involved in the generation of the McGurk effect, it remains unclear whether this region is critical only for this illusion or also for the more general benefits of congruent visual speech (e.g., increased accuracy and faster reaction times). Indeed, recent correlative research suggests that the benefits of congruent visual speech and the McGurk effect reflect largely independent mechanisms. To better understand how these different features of audiovisual integration are causally generated by the left pSTS, we used single-pulse TMS to temporarily impair processing while subjects were presented with either incongruent (McGurk) or congruent audiovisual combinations. Consistent with past research, we observed that TMS to the left pSTS significantly reduced the strength of the McGurk effect. Importantly, however, left pSTS stimulation did not affect the positive benefits of congruent audiovisual speech (increased accuracy and faster reaction times), demonstrating a causal dissociation between the two processes. Our results are consistent with models proposing that the pSTS is but one of multiple critical areas supporting audiovisual speech interactions. Moreover, these data add to a growing body of evidence suggesting that the McGurk effect is an imperfect surrogate measure for more general and ecologically valid audiovisual speech behaviors.

neuroscience↗

Auditory cortex encodes lipreading information through spatially distributed activity

Watching a speakers face improves speech perception accuracy. These benefits are owed, in part, to implicit lipreading abilities present in the general population. While it is established that lipreading can alter the perception of a heard word, it is unknown how information that is extracted from lipread words is transformed into a neural code that the auditory system can use. One influential, but untested, hypothesis is that visual speech modulates the population coded representations of phonetic and phonemic features in the auditory system. This model is largely supported by data showing that silent lipreading evokes activity in auditory cortex, but these activations could alternatively reflect general effects of arousal or attention, or the encoding of non-linguistic features such as visual timing information. This gap limits our understanding of how vision supports speech perception processes. To test the hypothesis that the auditory system encodes visual speech information, we acquired fMRI data from healthy adults and intracranial recordings from electrodes implanted in patients with epilepsy during auditory and visual speech perception tasks. Across both methods, linear classifiers successfully decoded the identity of silently lipread words using the spatial pattern of auditory cortex responses. Examining the time-course of classification using intracranial recordings, lipread words were classified at significantly earlier time-points relative to heard words, suggesting a predictive mechanism for facilitating speech. These results support a model in which the auditory system combines the joint neural distributions evoked by heard and lipread words to generate a more precise estimate of what was said. Significance StatementWhen we listen to someone speak in a noisy environment, watching their face can help us understand them better, largely due to automatic lipreading abilities. However, it unknown how lipreading information is transformed into a neural code that the auditory system can use. We used fMRI and intracranial recordings in patients to study how the brain processes silently lipread words and found that the auditory system encodes the identity of lipread words through spatially distributed activity. These results suggest that the auditory system combines information from both lipreading and hearing to generate more precise estimates of what is said, potentially by both activating the corresponding representation of the heard word and suppressing incorrect phonemic representations.

neuroscience↗

Functional alterations in cortical processing of speech in glioma-infiltrated cortex

Recent developments in the biology of malignant gliomas have demonstrated that glioma cells interact with neurons through both paracrine signaling and electrochemical synapses. Glioma-neuron interactions consequently modulate the excitability of local neuronal circuits, and it is unclear the extent to which glioma-infiltrated cortex can meaningfully participate in neural computations. For example, gliomas may result in a local disorganization of activity that impedes the transient synchronization of neural oscillations. Alternatively, glioma-infiltrated cortex may retain the ability to engage in synchronized activity, in a manner similar to normal-appearing cortex, but exhibit other altered spatiotemporal patterns of activity with subsequent impact on cognitive processing. Here, we use subdural electrocorticography to sample both normal-appearing and glioma-infiltrated cortex during speech. We find that glioma-infiltrated cortex engages in synchronous activity during task performance in a manner similar to normal-appearing cortex, but recruits a diffuse spatial network. On a temporal scale, we show that glioma-infiltrated cortex has lower capacity for information encoding when performing nuanced tasks such as speech production of monosyllabic versus polysyllabic words. As a result, temporal decoding strategies for distinguishing monosyllabic from polysyllabic words were feasible for signals arising from normal-appearing cortex, but not from glioma-infiltrated cortex. These findings inform our understanding of cognitive processing in chronic disease states and have implications for neuromodulation and prosthetics in patients with malignant gliomas. Significance StatementAs gliomas proliferate, they infiltrate healthy brain tissue. Often, patients with such tumors in the language areas of the brain develop aphasia. Understanding how gliomas interact with normal neural circuits is critical for developing neuroprostheses that restore speech. Recent evidence demonstrates that glioma cells interact synaptically with neurons, and thus can modulate neural circuits. However, it is unclear the extent to which glioma-infiltrated cortex participates in cognitive processing. Using electrocorticography to record both glioma-infiltrated and normal-appearing cortex during speech, we found that glioma-infiltrated cortex is capable of coordinated neural responses, but has reduced capacity for information encoding. Instead, glioma-infiltrated cortex recruits a broader network of cortical regions during speech, which may represent a compensatory mechanism with implications for future neuroprostheses.

neuroscience↗

Glioblastoma remodeling of neural circuits in the human brain decreases survival

Gliomas synaptically integrate into neural circuits. Prior work has demonstrated bidirectional interactions between neurons and glioma cells, with neuronal activity driving glioma growth and gliomas increasing neuronal excitability. In this study we wanted to know how glioma induced neuronal changes influence neural circuits underlying cognition and whether these interactions influence patient survival. We use intracranial brain recordings during lexical retrieval language tasks in awake humans in addition to site specific tumor tissue biopsies and cell biology experiments. We find that gliomas remodel functional neural circuitry such that task-relevant neural responses activate tumor-infiltrated cortex, beyond cortical excitation normally recruited in the healthy brain. Site-directed biopsies from functionally connected regions within the tumor are enriched for a glioblastoma subpopulation that exhibits a distinct synaptogenic and neuronotrophic phenotype. Tumor cells from functionally connected regions secrete the synaptogenic factor thrombospondin-1, which contributes to the differential neuron-glioma interactions observed in functionally connected tumor regions compared to tumor regions with less functional connectivity. The degree of functional connectivity between glioblastoma and the normal brain negatively impacts both patient survival and language task performance. These data demonstrate that high-grade gliomas functionally remodel neural circuits in the human brain, which both promotes tumor proliferation and impairs cognition.

cancer biology↗

Convergence of Heteromodal Lexical Retrieval in the Lateral Prefrontal Cortex

Lexical retrieval requires selecting and retrieving the most appropriate word from the lexicon to express a desired concept. Prior studies investigating the neuroanatomic underpinnings of lexical retrieval used lesion models that rely on stereotyped vascular distributions, functional neuroimaging methods that lack causal certainty, or awake brain mapping that is typically limited to narrow cortical exposures. Further, few studies have probed lexical retrieval with tasks other than picture naming and when non-picture naming lexical retrieval tasks have been applied, both convergent and divergent models emerged. Because of this existing controversy, we set out to test the hypothesis that cortical and subcortical brain regions specifically involved in lexical retrieval in response to visual and auditory stimuli represent overlapping neural systems. Fifty-three patients with dysnomic aphasia due to dominant-hemisphere brain tumors performed four language tasks: picture naming, auditory naming, text reading, and describing line drawings with correct syntax. A subset of participants also underwent the Quick Aphasia Battery which provides a validated measure of lexical retrieval via the word finding subtest. Generalized linear modeling and principal components analysis revealed multicollinearity between picture naming, auditory naming, and word finding, implying redundancies between the linguistic measures. Support vector regression lesion-symptom mapping across participants was used to model accuracies on each of the four language tasks. Picture naming and auditory naming survived cluster-level corrections. Specifically, lesions within overlapping clusters of 8,333 voxels and 21,512 voxels in the left lateral PFC were predictive of impaired picture naming and auditory naming, respectively. These data indicate a convergence of heteromodal lexical retrieval within the PFC. Importance of the StudyLexical retrieval (i.e., selecting and retrieving words to convey desired concepts) is a crucial component of language processing. However, existing studies of the neuroanatomic underpinnings of lexical retrieval lack causal relationships and have provided conflicting evidence, suggesting both convergent and divergent models. In order to resolve these conflicting models, we used lesion-symptom mapping to investigate lexical retrieval in 53 patients with dominant-hemisphere brain tumors. We observed significant associations between performance on visual and auditory naming tasks. Further, performance on these tasks predicted performance on a validated neuropsychological measure of lexical retrieval. Critically, multivariate, nonparametric lesion-symptom mapping within a brain tumor framework revealed that lesions in overlapping regions of the left lateral prefrontal cortex (PFC) predict impaired visual and auditory naming. In a clinical context, this approach to identifying causal brain-behavior relationships could help to guide brain tumor therapies such as cytoreductive surgery and supportive rehabilitation services.

neuroscience↗

Auditory-Visual Speech Behaviors are Resilient to Left pSTS Damage

The ability to understand spoken language is essential for social, vocational, and emotional health, but can be disrupted by environmental noise, injury, or hearing loss. These auditory deficits can be ameliorated by visual speech signals that convey redundant or supplemental speech information, but the brain regions critically responsible for these audiovisual (AV) interactions remain poorly understood. Previous TMS and lesion-mapping studies suggest that the left posterior superior temporal sulcus (pSTS) is causally implicated in producing the McGurk effect, an AV illusion in which auditory and visual speech are perceptually "fused." However, previous research suggests that the McGurk effect is neurally and behaviorally dissociable from other visual effects on speech perception and, therefore, may not provide a generalizable index of AV interactions in speech perception more broadly. To examine whether the left pSTS is critically responsible for AV speech integration more broadly, we measured the strength of the McGurk effect, AV facilitation effects, and AV conflict effects longitudinally over 2 years in patients undergoing surgery for intrinsic tumors in the left pSTS (n = 2) or frontal lobes (control; n = 14). Results demonstrated that left pSTS lesions impaired experience of the McGurk effect, but did not uniformly reduce visual influences on speech perception. Additionally, when multisensory behaviors were affected by a lesion, AV speech perception abilities could recover over time. Our results suggest a causal dissociation between perceptual benefits produced by congruent AV speech and perceptual modulations produced by incongruent AV speech (the McGurk effect).These data are consistent with models proposing that that the pSTS is only one of multiple critical areas necessary for AV speech interactions.

neuroscience↗

Visual speech differentially modulates beta, theta, and high gamma bands in auditory cortex

Speech perception is a central component of social communication. While principally an auditory process, accurate speech perception in everyday settings is supported by meaningful information extracted from visual cues (e.g., speech content, timing, and speaker identity). Previous research has shown that visual speech modulates activity in cortical areas subserving auditory speech perception, including the superior temporal gyrus (STG), potentially through feedback connections from the multisensory posterior superior temporal sulcus (pSTS). However, it is unknown whether visual modulation of auditory processing in the STG is a unitary phenomenon or, rather, consists of multiple temporally, spatially, or functionally distinct processes. To explore these questions, we examined neural responses to audiovisual speech measured from intracranially implanted electrodes within the temporal cortex of 21 patients undergoing clinical monitoring for epilepsy. We found that visual speech modulates auditory processes in the STG in multiple ways, eliciting temporally and spatially distinct patterns of activity that differ across theta, beta, and high-gamma frequency bands. Before speech onset, visual information increased high-gamma power in the posterior STG and suppressed beta power in mid-STG regions, suggesting crossmodal prediction of speech signals in these areas. After sound onset, visual speech decreased theta power in the middle and posterior STG, potentially reflecting a decrease in sustained feedforward auditory activity. These results are consistent with models that posit multiple distinct mechanisms supporting audiovisual speech perception and provide a crucial map for subsequent studies to identify the types of visual features that are encoded by these separate mechanisms.

neuroscience↗