Parallel and distributed encoding of speech across human auditory cortex

Hamilton, Liberty S.; Oganian, Yulia; Hall, Jeffery A.; Chang, Edward F.

doi:10.1016/j.cell.2021.07.019

Cited by 136 publications

(177 citation statements)

References 110 publications

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“…STGP had an intermediate position of between HGPM and HGAL/PT/STGM in terms of its distance to center of embedding space and mean connectivity. This finding is consistent with the interpretation of STGP as the locus of relatively early non-core auditory cortex 60, 61 and occupying a low-level position similar to HGPM in one of the multiple parallel processing streams for speech 62 .…”

Section: Discussionsupporting

confidence: 91%

“…Importantly, subcortical structures, such as the thalamus, that link sensory and higher order networks 94 , were not sampled in these subjects. The functional organization presented here is likely influenced indirectly by the multiple thalamo-cortical pathways carrying lemniscal and extralemniscal sensory information to cortex 62,95 . Although previous fMRI studies of RS networks focused exclusively on cortical ROIs and did not consider the role of the thalamus and other subcortical structures, these studies have yielded valuable insights into the functional organization of the human cortical networks 96,97 .…”

Section: Caveats and Limitationsmentioning

confidence: 99%

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Functional geometry of auditory cortical resting state networks derived from intracranial electrophysiology

Banks

Krause

Berger

et al. 2022

Preprint

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Critical details remain unresolved about the organization of the human auditory cortical hierarchy and its relationship to higher order brain networks. We investigated this organization using diffusion map embedding (DME) applied to resting state intracranial electroencephalography (iEEG) obtained in neurosurgical patients. DME was applied to functional connectivity measured between regions of interest (ROIs). ROIs exhibited a hierarchical organization, symmetric between the two hemispheres and robust to the choice of iEEG frequency band, connectivity metric, and imaging modality. Tight clusters of canonical auditory and prefrontal ROIs were maximally segregated in embedding space. Clusters consistent with ventral and dorsal auditory processing streams were paralleled by a cluster suggestive of a third stream linking auditory and limbic structures. Portions of anterior temporal cortex were characterized as global hubs. This approach lays the foundation for elucidating network changes underlying transitions of arousal state, disorders of consciousness, and during active speech and language processing.

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Section: Discussionsupporting

confidence: 91%

Section: Caveats and Limitationsmentioning

confidence: 99%

Functional geometry of auditory cortical resting state networks derived from intracranial electrophysiology

Banks

Krause

Berger

et al. 2022

Preprint

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“…Proof of principle results from one patient demonstrated significant auditory encoding of the acoustic envelope in high gamma activity. The relatively low correlations of the model are likely a result of the locations of the electrodes in this particular patient – higher performance would be expected for electrodes in the superior temporal gyrus and Heschl’s gyrus ( Hamilton et al, 2021 ; Khalighinejad et al, 2021 ). However, more lateral electrodes (higher numbers on each device) generally showed better envelope following, which is consistent with what we would expect based on functional neuroanatomy.…”

Section: Discussionmentioning

confidence: 95%

A Platform for Cognitive Monitoring of Neurosurgical Patients During Hospitalization

Ashmaig

Hamilton

Modur

et al. 2021

Front. Hum. Neurosci.

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Intracranial recordings in epilepsy patients are increasingly utilized to gain insight into the electrophysiological mechanisms of human cognition. There are currently several practical limitations to conducting research with these patients, including patient and researcher availability and the cognitive abilities of patients, which limit the amount of task-related data that can be collected. Prior studies have synchronized clinical audio, video, and neural recordings to understand naturalistic behaviors, but these recordings are centered on the patient to understand their seizure semiology and thus do not capture and synchronize audiovisual stimuli experienced by patients. Here, we describe a platform for cognitive monitoring of neurosurgical patients during their hospitalization that benefits both patients and researchers. We provide the full specifications for this system and describe some example use cases in perception, memory, and sleep research. We provide results obtained from a patient passively watching TV as proof-of-principle for the naturalistic study of cognition. Our system opens up new avenues to collect more data per patient using real-world behaviors, affording new possibilities to conduct longitudinal studies of the electrophysiological basis of human cognition under naturalistic conditions.

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“…The auditory system is involved in a number of crucial sensory functions, including speech processing (Hamilton et al 2021), (Matsumoto et al 2011), (Fontolan et al 2014), (Gourévitch et al 2008), sound localization (Andéol et al 2011), (Carlile, Martin, and McAnally 2005), (Ahveninen, Kopčo, and Jääskeläinen 2014), pitch discrimination (Tramo, Shah, and Braida 2002), (Tramo et al 2005), (Dykstra et al 2012), (Hyde, Peretz, and Zatorre 2008), and voice recognition (Latinus et al 2013), (Holmes and Johnsrude 2021). Aberrations along this pathway can result in a wide variety of pathologies.…”

Section: Introductionmentioning

confidence: 99%

Data-driven multiscale model of macaque auditory thalamocortical circuits reproduces in vivo dynamics

Durá-Bernal

Griffith

Barczak

et al. 2022

Preprint

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We developed a biophysically-detailed model of the macaque auditory thalamocortical circuits, including primary auditory cortex (A1), medial geniculate body (MGB) and thalamic reticular nuclei (TRN), using the NEURON simulator and NetPyNE multiscale modeling tool. We simulated A1 as a cortical column with a depth of 2000 μm and 200 μm diameter, containing over 12k neurons and 30M synapses. Neuron densities, laminar locations, classes, morphology and biophysics, and connectivity at the long-range, local and dendritic scale were derived from published experimental data. The A1 model included 6 cortical layers and multiple populations of neurons consisting of 4 excitatory and 4 inhibitory types, and was reciprocally connected to the thalamus (MGB and TRN) mimicking anatomical connectivity. MGB included core and matrix thalamocortical neurons with layer-specific projection patterns to A1, and thalamic interneurons projecting locally. Auditory stimulus related inputs were simulated using phenomenological models of the cochlear auditory nerve and the inferior colliculus, which served as input to MGB. The model generated cell type and layer-specific firing rates consistent with overall ranges observed experimentally, and accurately simulated the corresponding local field potentials (LFPs), current source density (CSD), and electroencephalogram (EEG) signals. Laminar CSD patterns during spontaneous activity and responses to speech input were similar to those recorded experimentally. Physiological oscillations emerged spontaneously across frequency bands without external rhythmic inputs and were comparable to those recorded in vivo. We used the model to unravel the contributions from distinct cell type and layer-specific neuronal populations to oscillation events detected in CSD, and explore how these relate to the population firing patterns. Overall, the computational model provides a quantitative theoretical framework to integrate and interpret a wide range of experimental data in auditory circuits. It also constitutes a powerful tool to evaluate hypotheses and make predictions about the cellular and network mechanisms underlying common experimental measurements, including MUA, LFP and EEG signals.

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Parallel and distributed encoding of speech across human auditory cortex

Cited by 136 publications

References 110 publications

Functional geometry of auditory cortical resting state networks derived from intracranial electrophysiology

Functional geometry of auditory cortical resting state networks derived from intracranial electrophysiology

A Platform for Cognitive Monitoring of Neurosurgical Patients During Hospitalization

Data-driven multiscale model of macaque auditory thalamocortical circuits reproduces in vivo dynamics

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