Plos Biology Feb 2022,

A cortical network processes auditory error signals during human speech production to maintain fluency

Müge Özker, Werner K Doyle, Orrin Devinsky, Adeen Flinker
Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however, the underlying neural mechanisms are still poorly understood. Computational models of speech motor control suggest that, during speech production, the brain uses an efference copy of the motor command to generate an internal estimate of the speech output. When actual feedback differs from this internal estimate, an error signal is generated to correct the internal estimate and update necessary motor commands to produce intended speech. We were able to localize the auditory error signal using electrocorticographic recordings from neurosurgical participants during a delayed auditory feedback (DAF) paradigm. In this task, participants hear their voice with a time delay as they produced words and sentences (similar to an echo on a conference call), which is well known to disrupt fluency by causing slow and stutter-like speech in humans. We observed a significant response enhancement in auditory cortex that scaled with the duration of feedback delay, indicating an auditory speech error signal. Immediately following auditory cortex, dorsal precentral gyrus (dPreCG), a region that has not been implicated in auditory feedback processing before, exhibited a markedly similar response enhancement, suggesting a tight coupling between the 2 regions. Critically, response enhancement in dPreCG occurred only during articulation of long utterances due to a continuous mismatch between produced speech and reafferent feedback. These results suggest that dPreCG plays an essential role in processing auditory error signals during speech production to maintain fluency.
Neurology Aug 2020, 10.1212/WNL.0000000000010639; DOI: 10.1212/WNL.0000000000010639

Neural correlates of sign language production revealed by electrocorticography

Jennifer Shum, Lora Fanda, Patricia Dugan, Werner K Doyle, Orrin Devinsky, Adeen Flinker
Objective: The combined spatiotemporal dynamics underlying sign language production remains largely unknown. To investigate these dynamics as compared to speech production we utilized intracranial electrocorticography during a battery of language tasks.

Methods: We report a unique case of direct cortical surface recordings obtained from a neurosurgical patient with intact hearing and bilingual in English and American Sign Language. We designed a battery of cognitive tasks to capture multiple modalities of language processing and production.
Results: We identified two spatially distinct cortical networks: ventral for speech and dorsal for sign production. Sign production recruited peri-rolandic, parietal and posterior temporal regions, while speech production recruited frontal, peri-sylvian and peri-rolandic regions. Electrical cortical stimulation confirmed this spatial segregation, identifying mouth areas for speech production and limb areas for sign production. The temporal dynamics revealed superior parietal cortex activity immediately before sign production, suggesting its role in planning and producing sign language.

Conclusions: Our findings reveal a distinct network for sign language and detail the temporal propagation supporting sign production.

Spectrotemporal modulation provides a unifying framework for auditory cortical asymmetries

Flinker, Adeen; Doyle, Werner K; Mehta, Ashesh D; Devinsky, Orrin; Poeppel, David
The principles underlying functional asymmetries in cortex remain debated. For example, it is accepted that speech is processed bilaterally in auditory cortex, but a left hemisphere dominance emerges when the input is interpreted linguistically. The mechanisms, however, are contested, such as what sound features or processing principles underlie laterality. Recent findings across species (humans, canines and bats) provide converging evidence that spectrotemporal sound features drive asymmetrical responses. Typically, accounts invoke models wherein the hemispheres differ in time-frequency resolution or integration window size. We develop a framework that builds on and unifies prevailing models, using spectrotemporal modulation space. Using signal processing techniques motivated by neural responses, we test this approach, employing behavioural and neurophysiological measures. We show how psychophysical judgements align with spectrotemporal modulations and then characterize the neural sensitivities to temporal and spectral modulations. We demonstrate differential contributions from both hemispheres, with a left lateralization for temporal modulations and a weaker right lateralization for spectral modulations. We argue that representations in the modulation domain provide a more mechanistic basis to account for lateralization in auditory cortex.

Redefining the role of Broca’s area in speech

Flinker, Adeen; Korzeniewska, Anna; Shestyuk, Avgusta Y; Franaszczuk, Piotr J; Dronkers, Nina F; Knight, Robert T; Crone, Nathan E
For over a century neuroscientists have debated the dynamics by which human cortical language networks allow words to be spoken. Although it is widely accepted that Broca’s area in the left inferior frontal gyrus plays an important role in this process, it was not possible, until recently, to detail the timing of its recruitment relative to other language areas, nor how it interacts with these areas during word production. Using direct cortical surface recordings in neurosurgical patients, we studied the evolution of activity in cortical neuronal populations, as well as the Granger causal interactions between them. We found that, during the cued production of words, a temporal cascade of neural activity proceeds from sensory representations of words in temporal cortex to their corresponding articulatory gestures in motor cortex. Broca’s area mediates this cascade through reciprocal interactions with temporal and frontal motor regions. Contrary to classic notions of the role of Broca’s area in speech, while motor cortex is activated during spoken responses, Broca’s area is surprisingly silent. Moreover, when novel strings of articulatory gestures must be produced in response to nonword stimuli, neural activity is enhanced in Broca’s area, but not in motor cortex. These unique data provide evidence that Broca’s area coordinates the transformation of information across large-scale cortical networks involved in spoken word production. In this role, Broca’s area formulates an appropriate articulatory code to be implemented by motor cortex.

Single-trial speech suppression of auditory cortex activity in humans

Flinker, Adeen; Chang, Edward F; Kirsch, Heidi E; Barbaro, Nicholas M; Crone, Nathan E; Knight, Robert T
The human auditory cortex is engaged in monitoring the speech of interlocutors as well as self-generated speech. During vocalization, auditory cortex activity is reported to be suppressed, an effect often attributed to the influence of an efference copy from motor cortex. Single-unit studies in non-human primates have demonstrated a rich dynamic range of single-trial auditory responses to self-speech consisting of suppressed, nonsuppressed and excited auditory neurons. However, human research using noninvasive methods has only reported suppression of averaged auditory cortex responses to self-generated speech. We addressed this discrepancy by recording electrocorticographic activity from neurosurgical subjects performing auditory repetition tasks. We observed that the degree of suppression varied across different regions of auditory cortex, revealing a variety of suppressed and nonsuppressed responses during vocalization. Importantly, single-trial high-gamma power (gamma(High), 70-150 Hz) robustly tracked individual auditory events and exhibited stable responses across trials for suppressed and nonsuppressed regions.

Sub-centimeter language organization in the human temporal lobe

Flinker, A; Chang, E F; Barbaro, N M; Berger, M S; Knight, R T
The human temporal lobe is well known to be critical for language comprehension. Previous physiological research has focused mainly on non-invasive neuroimaging and electrophysiological techniques with each approach requiring averaging across many trials and subjects. The results of these studies have implicated extended anatomical regions in peri-sylvian cortex in speech perception. These non-invasive studies typically report a spatially homogenous functional pattern of activity across several centimeters of cortex. We examined the spatiotemporal dynamics of word processing using electrophysiological signals acquired from high-density electrode arrays (4mm spacing) placed directly on the human temporal lobe. Electrocorticographic (ECoG) activity revealed a rich mosaic of language activity, which was functionally distinct at four mm separation. Cortical sites responding specifically to word and not phoneme stimuli were surrounded by sites that responded to both words and phonemes. Other sub-regions of the temporal lobe responded robustly to self-produced speech and minimally to external stimuli while surrounding sites at 4mm distance exhibited an inverse pattern of activation. These data provide evidence for temporal lobe specificity to words as well as self-produced speech. Furthermore, the results provide evidence that cortical processing in the temporal lobe is not spatially homogenous over centimeters of cortex. Rather, language processing is supported by independent and spatially distinct functional sub-regions of cortex at a resolution of at least 4mm.