The peri-Sylvian cortical network underlying single word repetition revealed by electrocortical stimulation and direct neural recordings

Leonard, Matthew K.; Cai, Ruofan; Babiak, Miranda; Ren, Angela; Chang, Edward F.

doi:10.1016/j.bandl.2016.06.001

Cited by 45 publications

(44 citation statements)

References 66 publications

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“…NMF is particularly useful for decomposing data into "parts" that have interpretable meanings (e.g., transient vs sustained response types) (Lee and Seung, 1999;Donoho and Stodden, 2004;Bouchard et al, 2016;Leonard et al, 2016). The HG activity for each vSMC electrode across all participants was averaged across trials, offset by the minimum value (such that all values were positive), and NMF was applied to the matrix of time courses ϫ electrodes.…”

Section: Discussionmentioning

confidence: 99%

Human Sensorimotor Cortex Control of Directly Measured Vocal Tract Movements during Vowel Production

et al. 2018

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During speech production, we make vocal tract movements with remarkable precision and speed. Our understanding of how the human brain achieves such proficient control is limited, in part due to the challenge of simultaneously acquiring high-resolution neural recordings and detailed vocal tract measurements. To overcome this challenge, we combined ultrasound and video monitoring of the supralaryngeal articulators (lips, jaw, and tongue) with electrocorticographic recordings from the cortical surface of 4 subjects (3 female, 1 male) to investigate how neural activity in the ventral sensory-motor cortex (vSMC) relates to measured articulator movement kinematics (position, speed, velocity, acceleration) during the production of English vowels. We found that high-gamma activity at many individual vSMC electrodes strongly encoded the kinematics of one or more articulators, but less so for vowel formants and vowel identity. Neural population decoding methods further revealed the structure of kinematic features that distinguish vowels. Encoding of articulator kinematics was sparsely distributed across time and primarily occurred during the time of vowel onset and offset. In contrast, encoding was low during the steady-state portion of the vowel, despite sustained neural activity at some electrodes. Significant representations were found for all kinematic parameters, but speed was the most robust. These findings enabled by direct vocal tract monitoring demonstrate novel insights into the representation of articulatory kinematic parameters encoded in the vSMC during speech production. Speaking requires precise control and coordination of the vocal tract articulators (lips, jaw, and tongue). Despite the impressive proficiency with which humans move these articulators during speech production, our understanding of how the brain achieves such control is rudimentary, in part because the movements themselves are difficult to observe. By simultaneously measuring speech movements and the neural activity that gives rise to them, we demonstrate how neural activity in sensorimotor cortex produces complex, coordinated movements of the vocal tract.

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Section: Discussionmentioning

confidence: 99%

Human Sensorimotor Cortex Control of Directly Measured Vocal Tract Movements during Vowel Production

et al. 2018

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“…An important goal for future research will be to understand the real-time dynamics of functional interactions between the right inferior frontal gyrus and right superior temporal gyrus when patients are repeating melodies and sentences. Future work with electrocorticography could study the dynamics that mediate interactions between the right superior temporal gyrus and right inferior frontal gyrus during melody and language processing (e.g., for evidence in the domain of language see [31–33]; for review, see [34–35]).…”

Section: Discussionmentioning

confidence: 99%

Direct Electrical Stimulation in the Human Brain Disrupts Melody Processing

et al. 2017

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Summary Prior research using functional magnetic resonance imaging (fMRI) [1–4] and behavioral studies of patients with acquired or congenital amusia [5–8] suggest that the right posterior superior temporal gyrus (STG) in the human brain is specialized for aspects of music processing (for review see 9–12). Intracranial electrical brain stimulation in awake neurosurgery patients is a powerful means to determine the computations supported by specific brain regions and networks [13–21], because it provides reversible causal evidence with high spatial resolution (for review, see [22, 23]). Prior intracranial stimulation or cortical cooling studies have investigated musical abilities related to reading music scores [13, 14] and singing familiar songs [24, 25]. However, individuals with amusia (congenitally, or from a brain injury) have difficulty humming melodies but can be spared for singing familiar songs with familiar lyrics [26]. Here we report a detailed study of a musician with a low-grade tumor in the right temporal lobe. Functional MRI was used pre-operatively to localize music processing to the right STG, and the patient subsequently underwent awake intraoperative mapping using direct electrical stimulation during a melody repetition task. Stimulation of the right STG induced ‘music arrest’ and errors in pitch, but did not affect language processing. These findings provide causal evidence for the functional segregation of music and language processing in the human brain, and confirm a specific role of the right STG in melody processing.

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“…2). In this study, we focused on the HG band given its strong association with cortical activation (Ray et al, 2008) and relevance for linguistic neurophysiology (Leonard et al, 2016a; Leonard et al, 2016b; Steinschneider et al, 2011), though analysis of lower frequency dynamics would also be possible with data acquired by the RNS System. Future experiments employing a more diverse array of tasks could determine the specificity of the observed responses for language, motor preparation, or other aspects of cognitive processing (Udden and Bahlmann, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…She underwent iEEG with left frontotemporal grid electrode coverage, and ictal recordings localized seizures to the posterior left STG. Both extraoperative (during inpatient seizure monitoring) and intraoperative (during grid explantation) electrical stimulation mapping revealed that the seizure onset zone encompassed eloquent language cortex, including parts of classical Wernicke’s area (Leonard et al, 2016b). This region was deemed unresectable, so the RNS System was implanted as an alternative treatment option.…”

Section: Methodsmentioning

confidence: 99%

Chronic ambulatory electrocorticography from human speech cortex

et al. 2017

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Direct intracranial recording of human brain activity is an important approach for deciphering neural mechanisms of cognition. Such recordings, usually made in patients with epilepsy undergoing inpatient monitoring for seizure localization, are limited in duration and depend on patients’ tolerance for the challenges associated with recovering from brain surgery. Thus, typical intracranial recordings, similar to most non-invasive approaches in humans, provide snapshots of brain activity in acute, highly constrained settings, limiting opportunities to understand long timescale and natural, real-world phenomena. A new device for treating some forms of drug-resistant epilepsy, the NeuroPace RNS® System, includes a cranially-implanted neurostimulator and intracranial electrodes that continuously monitor brain activity and respond to incipient seizures with electrical counterstimulation. The RNS System can record epileptic brain activity over years, but whether it can record meaningful, behavior-related physiological responses has not been demonstrated. Here, in a human subject with electrodes implanted over high-level speech-auditory cortex (Wernicke’s area; posterior superior temporal gyrus), we report that cortical evoked responses to spoken sentences are robust, selective to phonetic features, and stable over nearly 1.5 years. In a second subject with RNS System electrodes implanted over frontal cortex (Broca’s area, posterior inferior frontal gyrus), we found that word production during a naming task reliably evokes cortical responses preceding speech onset. The spatiotemporal resolution, high signal-to-noise, and wireless nature of this system’s intracranial recordings make it a powerful new approach to investigate the neural correlates of human cognition over long timescales in natural ambulatory settings.

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The peri-Sylvian cortical network underlying single word repetition revealed by electrocortical stimulation and direct neural recordings

Cited by 45 publications

References 66 publications

Human Sensorimotor Cortex Control of Directly Measured Vocal Tract Movements during Vowel Production

Human Sensorimotor Cortex Control of Directly Measured Vocal Tract Movements during Vowel Production

Direct Electrical Stimulation in the Human Brain Disrupts Melody Processing

Chronic ambulatory electrocorticography from human speech cortex

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