Biology subjects

Doyle, W.

Publications and source records attributed to Doyle, W..

At least 37 records · Page 2Linked to original sources

bioRxiv2023

Speech-induced suppression and vocal feedback sensitivity in human cortex

Across the animal kingdom, neural responses in the auditory cortex are suppressed during vocalization, and humans are no exception. A common hypothesis is that suppression increases sensitivity to auditory feedback, enabling the detection of vocalization errors. This hypothesis has been previously confirmed in non-human primates, however a direct link between auditory suppression and sensitivity in human speech monitoring remains elusive. To address this issue, we obtained intracranial electroencephalography (iEEG) recordings from 35 neurosurgical participants during speech production. We first characterized the detailed topography of auditory suppression, which varied across superior temporal gyrus (STG). Next, we performed a delayed auditory feedback (DAF) task to determine whether the suppressed sites were also sensitive to auditory feedback alterations. Indeed, overlapping sites showed enhanced responses to feedback, indicating sensitivity. Importantly, there was a strong correlation between the degree of auditory suppression and feedback sensitivity, suggesting suppression might be a key mechanism that underlies speech monitoring. Further, we found that when participants produced speech with simultaneous auditory feedback, posterior STG was selectively activated if participants were engaged in a DAF paradigm, suggesting that increased attentional load can modulate auditory feedback sensitivity.

neuroscience↗

bioRxiv2023

A Neural Speech Decoding Framework Leveraging Deep Learning and Speech Synthesis

Decoding human speech from neural signals is essential for brain-computer interface (BCI) technologies restoring speech function in populations with neurological deficits. However, it remains a highly challenging task, compounded by the scarce availability of neural signals with corresponding speech, data complexity, and high dimensionality, and the limited publicly available source code. Here, we present a novel deep learning-based neural speech decoding framework that includes an ECoG Decoder that translates electrocorticographic (ECoG) signals from the cortex into interpretable speech parameters and a novel differentiable Speech Synthesizer that maps speech parameters to spectrograms. We develop a companion audio-to-audio auto-encoder consisting of a Speech Encoder and the same Speech Synthesizer to generate reference speech parameters to facilitate the ECoG Decoder training. This framework generates natural-sounding speech and is highly reproducible across a cohort of 48 participants. Among three neural network architectures for the ECoG Decoder, the 3D ResNet model has the best decoding performance (PCC=0.804) in predicting the original speech spectrogram, closely followed by the SWIN model (PCC=0.796). Our experimental results show that our models can decode speech with high correlation even when limited to only causal operations, which is necessary for adoption by real-time neural prostheses. We successfully decode speech in participants with either left or right hemisphere coverage, which could lead to speech prostheses in patients with speech deficits resulting from left hemisphere damage. Further, we use an occlusion analysis to identify cortical regions contributing to speech decoding across our models. Finally, we provide open-source code for our two-stage training pipeline along with associated preprocessing and visualization tools to enable reproducible research and drive research across the speech science and prostheses communities.

neuroscience↗

bioRxiv2023

Timing and location of speech errors induced by direct cortical stimulation

Cortical regions supporting speech production are commonly established using neuroimaging techniques in both research and clinical settings. However, for neurosurgical purposes, structural function is routinely mapped peri-operatively using direct electrocortical stimulation. While this method is the gold standard for identification of eloquent cortical regions to preserve in neurosurgical patients, there is lack of specificity of the actual underlying cognitive processes being interrupted. To address this, we propose mapping the temporal dynamics of speech arrest across peri-sylvian cortices by quantifying the latency between stimulation and speech deficits. In doing so, we are able to substantiate hypotheses about distinct region-specific functional roles (e.g., planning versus motor execution). In this retrospective observational study, we analyzed 20 patients (12 female; age range 14-43) with refractory epilepsy who underwent continuous extra-operative intracranial EEG monitoring of an automatic speech task during clinical bedside language mapping. Latency to speech arrest was calculated as time from stimulation onset to speech arrest onset, controlling for individual speech rate. Most instances of motor-based arrest (87.5% of 96 instances) were in sensorimotor cortex with mid-range latencies to speech arrest with a distributional peak at 0.47 seconds. Speech arrest occurred in numerous regions, with relatively short latencies in supramarginal gyrus (0.46 seconds), superior temporal gyrus (0.51 seconds), and middle temporal gyrus (0.54 seconds), followed by relatively long latencies in sensorimotor cortex (0.72 seconds) and especially long latencies in inferior frontal gyrus (0.95 seconds). Nonparametric testing for speech arrest revealed that region predicted latency; latencies in supramarginal gyrus and in superior temporal gyrus were shorter than in sensorimotor cortex and in inferior frontal gyrus. Sensorimotor cortex is primarily responsible for motor-based arrest. Latencies to speech arrest in supramarginal gyrus and superior temporal gyrus (and to a lesser extent middle temporal gyrus) align with latencies to motor-based arrest in sensorimotor cortex. This pattern of relatively quick cessation of speech suggests that stimulating these regions interferes with the outgoing motor execution. In contrast, the latencies to speech arrest in inferior frontal gyrus and in ventral regions of sensorimotor cortex were significantly longer than those in temporoparietal regions. Longer latencies in the more frontal areas (including inferior frontal gyrus and ventral areas of precentral gyrus and postcentral gyrus) suggest that stimulating these areas interrupts a higher-level speech production process involved in planning. These results implicate the ventral specialization of sensorimotor cortex (including both precentral and postcentral gyri) for speech planning above and beyond motor execution.

neuroscience↗

bioRxiv2023

Temporal dynamics of neural adaptation across human visual cortex

Neural responses in visual cortex adapt to prolonged and repeated stimuli. While adaptation occurs across the visual cortex, it is unclear how adaptation patterns and computational mechanisms differ across the visual hierarchy. Here we characterize two signatures of short-term neural adaptation in time-varying intracranial electroencephalography (iEEG) data collected while participants viewed naturalistic image categories varying in duration and repetition interval. Ventraland lateral-occipitotemporal cortex exhibit slower and prolonged adaptation to single stimuli and slower recovery from adaptation to repeated stimuli compared to V1-V3. For category-selective electrodes, recovery from adaptation is slower for preferred than non-preferred stimuli. To model neural adaptation we augment our delayed divisive normalization (DN) model by scaling the input strength as a function of stimulus category, enabling the model to accurately predict neural responses across multiple image categories. The model fits suggest that differences in adaptation patterns arise from slower normalization dynamics in higher visual areas interacting with differences in input strength resulting from category selectivity. Our results reveal systematic differences in temporal adaptation of neural population responses across the human visual hierarchy and show that a single computational model of history-dependent normalization dynamics, fit with area-specific parameters, accounts for these differences. Author summaryNeural responses in visual cortex adapt over time, with reduced responses to prolonged and repeated stimuli. Here, we examine how adaptation patterns differ across the visual hierarchy in neural responses recorded from human visual cortex with high temporal and spatial precision. To identify possible neural computations underlying short-term adaptation, we fit the response time courses using a temporal divisive normalization model. The model accurately predicts prolonged and repeated responses in lower and higher visual areas, and reveals differences in temporal adaptation across the visual hierarchy and stimulus categories. Our model suggests that differences in adaptation patterns result from differences in divisive normalization dynamics. Our findings shed light on how information is integrated in the brain on a millisecond-time scale and offer an intuitive framework to study the emergence of neural dynamics across brain areas and stimuli.

neuroscience↗

bioRxiv2023

A shared linguistic space for transmitting our thoughts from brain to brain in natural conversations

Effective communication hinges on a mutual understanding of word meaning in different contexts. The embedding space learned by large language models can serve as an explicit model of the shared, context-rich meaning space humans use to communicate their thoughts. We recorded brain activity using electrocorticography during spontaneous, face-to-face conversations in five pairs of epilepsy patients. We demonstrate that the linguistic embedding space can capture the linguistic content of word-by-word neural alignment between speaker and listener. Linguistic content emerged in the speakers brain before word articulation, and the same linguistic content rapidly reemerged in the listeners brain after word articulation. These findings establish a computational framework to study how human brains transmit their thoughts to one another in real-world contexts.

neuroscience↗

bioRxiv2023

Deep speech-to-text models capture the neural basis of spontaneous speech in everyday conversations

Humans effortlessly use the continuous acoustics of speech to communicate rich linguistic meaning during everyday conversations. In this study, we leverage 100 hours (half a million words) of spontaneous open-ended conversations and concurrent high-quality neural activity recorded using electrocorticography (ECoG) to decipher the neural basis of real-world speech production and comprehension. Employing a deep multimodal speech-to-text model named Whisper, we develop encoding models capable of accurately predicting neural responses to both acoustic and semantic aspects of speech. Our encoding models achieved high accuracy in predicting neural responses in hundreds of thousands of words across many hours of left-out recordings. We uncover a distributed cortical hierarchy for speech and language processing, with sensory and motor regions encoding acoustic features of speech and higher-level language areas encoding syntactic and semantic information. Many electrodes--including those in both perceptual and motor areas--display mixed selectivity for both speech and linguistic features. Notably, our encoding model reveals a temporal progression from language-to-speech encoding before word onset during speech production and from speech-to-language encoding following word articulation during speech comprehension. This study offers a comprehensive account of the unfolding neural responses during fully natural, unbounded daily conversations. By leveraging a multimodal deep speech recognition model, we highlight the power of deep learning for unraveling the neural mechanisms of language processing in real-world contexts.

neuroscience↗

bioRxiv2023

Spatial Tuning of Alpha Oscillations in Human Visual Cortex

AO_SCPLOWBSTRACTC_SCPLOWNeuronal oscillations at about 10 Hz, called alpha oscillations, are often thought to arise from synchronous activity across occipital cortex, reflecting general cognitive states such as arousal and alertness. However, there is also evidence that modulation of alpha oscillations in visual cortex can be spatially specific. Here, we used intracranial electrodes in human patients to measure alpha oscillations in response to visual stimuli whose location varied systematically across the visual field. We separated the alpha oscillatory power from broadband power changes. The variation in alpha oscillatory power with stimulus position was then fit by a population receptive field (pRF) model. We find that the alpha pRFs have similar center locations to pRFs estimated from broadband power (70-180 Hz) but are several times larger. The results demonstrate that alpha suppression in human visual cortex can be precisely tuned. Finally, we show how the pattern of alpha responses can explain several features of exogenous visual attention. Significance StatementThe alpha oscillation is the largest electrical signal generated by the human brain. An important question in systems neuroscience is the degree to which this oscillation reflects system-wide states and behaviors such as arousal, alertness, and attention, versus much more specific functions in the routing and processing of information. We examined alpha oscillations at high spatial precision in human patients with intracranial electrodes implanted over visual cortex. We discovered a surprisingly high spatial specificity of visually driven alpha oscillations, which we quantified with receptive field models. We further use our discoveries about properties of the alpha response to show a link between these oscillations and the spread of visual attention. Grant support: NIH R01 MH111417 (Petridou, Winawer, Ramsey, Devinsky); JSPS Overseas Research Fellowship (Yuasa) The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health

neuroscience↗

bioRxiv2022

A Corollary Discharge Circuit in Human Speech

When we vocalize, our brain distinguishes self-generated sounds from external ones. A corollary discharge signal supports this function in animals, however, in humans its exact origin and temporal dynamics remain unknown. We report Electrocorticographic (ECoG) recordings in neurosurgical patients and a novel connectivity approach based on Granger-causality that reveals major neural communications. We find a reproducible source for corollary discharge across multiple speech production paradigms localized to ventral speech motor cortex before speech articulation. The uncovered discharge predicts the degree of auditory cortex suppression during speech, its well-documented consequence. These results reveal the human corollary discharge source and timing with far-reaching implication for speech motor-control as well as auditory hallucinations in human psychosis. Significance statementHow do organisms dissociate self-generated sounds from external ones? A fundamental brain circuit across animals addresses this question by transmitting a blueprint of the motor signal to sensory cortices, referred to as a corollary discharge. However, in humans and non-human primates auditory system, the evidence supporting this circuit has been limited to its direct consequence, auditory suppression. Furthermore, an impaired corollary discharge circuit in humans can lead to auditory hallucinations. While hypothesized to originate in the frontal cortex, direct evidence localizing the source and timing of an auditory corollary discharge is lacking in humans. Leveraging rare human neurosurgical recordings combined with connectivity techniques, we elucidate the exact source and dynamics of the corollary discharge signal in human speech. One-sentence summaryWe reveal the source and timing of a corollary discharge from speech motor cortex onto auditory cortex in human speech.

neuroscience↗

bioRxiv2022

Correspondence between the layered structure of deep language models and temporal structure of natural language processing in the human brain

Deep language models (DLMs) provide a novel computational paradigm for how the brain processes natural language. Unlike symbolic, rule-based models described in psycholinguistics, DLMs encode words and their context as continuous numerical vectors. These "embeddings" are constructed by a sequence of computations organized in "layers" to ultimately capture surprisingly sophisticated representations of linguistic structures. How does this layered hierarchy map onto the human brain during natural language comprehension? In this study, we used electrocorticography (ECoG) to record neural activity in language areas along the superior temporal gyrus and inferior frontal gyrus while human participants listened to a 30-minute spoken narrative. We supplied this same narrative to a high-performing DLM (GPT2-XL) and extracted the contextual embeddings for each word in the story across all 48 layers of the model. We next trained a set of linear encoding models to predict the temporally-evolving neural activity from the embeddings at each layer. We found a striking correspondence between the layer-by-layer sequence of embeddings from GPT2-XL and the temporal sequence of neural activity in language areas. In addition, we found evidence for the gradual accumulation of recurrent information along the linguistic processing hierarchy. However, we also noticed additional neural processes in the brain, but not in DLMs, during the processing of surprising (unpredictable) words. These findings point to a connection between human language processing and DLMs where the layer-by-layer accumulation of contextual information in DLM embeddings matches the temporal dynamics of neural activity in high-order language areas.

neuroscience↗

bioRxiv2022

Brain embeddings with shared geometry to artificial contextual embeddings, as a code for representing language in the human brain

Contextual embeddings, derived from deep language models (DLMs), provide a continuous vectorial representation of language. This embedding space differs fundamentally from the symbolic representations posited by traditional psycholinguistics. Do language areas in the human brain, similar to DLMs, rely on a continuous embedding space to represent language? To test this hypothesis, we densely recorded the neural activity in the Inferior Frontal Gyrus (IFG, also known as Brocas area) of three participants using dense intracranial arrays while they listened to a 30-minute podcast. From these fine-grained spatiotemporal neural recordings, we derived for each patient a continuous vectorial representation for each word (i.e., a brain embedding). Using stringent, zero-shot mapping, we demonstrated that brain embeddings in the IFG and the DLM contextual embedding space have strikingly similar geometry. This shared geometry allows us to precisely triangulate the position of unseen words in both the brain embedding space (zero-shot encoding) and the DLM contextual embedding space (zero-shot decoding). The continuous brain embedding space provides an alternative computational framework for how natural language is represented in cortical language areas.

neuroscience↗

bioRxiv2021

Distributed Feedforward and Feedback Processing across Perisylvian Cortex Supports Human Speech

Speech production is a complex human function requiring continuous feedforward commands together with reafferent feedback processing. These processes are carried out by distinct frontal and posterior cortical networks, but the degree and timing of their recruitment and dynamics remain unknown. We present a novel deep learning architecture that translates neural signals recorded directly from cortex to an interpretable representational space that can reconstruct speech. We leverage state-of-the-art learnt decoding networks to disentangle feedforward vs. feedback processing. Unlike prevailing models, we find a mixed cortical architecture in which frontal and temporal networks each process both feedforward and feedback information in tandem. We elucidate the timing of feedforward and feedback related processing by quantifying the derived receptive fields. Our approach provides evidence for a surprisingly mixed cortical architecture of speech circuitry together with decoding advances that have important implications for neural prosthetics.

neuroscience↗

bioRxiv2021

Temporal dynamics of neural responses in human visual cortex

Neural responses to visual stimuli exhibit complex temporal dynamics, including sub-additive temporal summation, response reduction with repeated or sustained stimuli (adaptation), and slower dynamics at low contrast. These phenomena are often studied independently. Here, we demonstrate these phenomena within the same experiment and model the underlying neural computations with a single computational model. We extracted time-varying responses from electrocorticographic (ECoG) recordings from patients presented with stimuli that varied in contrast, duration, and inter-stimulus interval (ISI). Aggregating data across patients yielded 98 electrodes with robust visual responses, covering both earlier (V1-V3) and higher-order (V3a/b, LO, TO, IPS) retinotopic maps. In all regions, the temporal dynamics of neural responses exhibit several non-linear features: peak response amplitude saturates with high contrast and longer stimulus durations; the response to a second stimulus is suppressed for short ISIs and recovers for longer ISIs; response latency decreases with increasing contrast. These features are accurately captured by a computational model comprised of a small set of canonical neuronal operations: linear filtering, rectification, exponentiation, and a delayed divisive normalization. We find that an increased normalization term captures both contrast- and adaptation-related response reductions, suggesting potentially shared underlying mechanisms. We additionally demonstrate both changes and invariance in temporal response dynamics between earlier and higher-order visual areas. Together, our results reveal the presence of a wide range of temporal and contrast-dependent neuronal dynamics in the human visual cortex, and demonstrate that a simple model captures these dynamics at millisecond resolution. Significance StatementSensory inputs and neural responses change continuously over time. It is especially challenging to understand a system that has both dynamic inputs and outputs. Here we use a computational modeling approach that specifies computations to convert a time-varying input stimulus to a neural response time course, and use this to predict neural activity measured in the human visual cortex. We show that this computational model predicts a wide variety of complex neural response shapes that we induced experimentally by manipulating the duration, repetition and contrast of visual stimuli. By comparing data and model predictions, we uncover systematic properties of temporal dynamics of neural signals, allowing us to better understand how the brain processes dynamic sensory information.

neuroscience↗

bioRxiv2021

Spontaneous neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Spontaneous fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on invasive electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

neuroscience↗

bioRxiv2020

Thinking ahead: prediction in context as a keystone of language in humans and machines

Departing from traditional linguistic models, advances in deep learning have resulted in a new type of predictive (autoregressive) deep language models (DLMs). Using a self-supervised next-word prediction task, these models are trained to generate appropriate linguistic responses in a given context. We provide empirical evidence that the human brain and autoregressive DLMs share three fundamental computational principles as they process natural language: 1) both are engaged in continuous next-word prediction before word-onset; 2) both match their pre-onset predictions to the incoming word to calculate post-onset surprise (i.e., prediction error signals); 3) both represent words as a function of the previous context. In support of these three principles, our findings indicate that: a) the neural activity before word-onset contains context-dependent predictive information about forthcoming words, even hundreds of milliseconds before the words are perceived; b) the neural activity after word-onset reflects the surprise level and prediction error; and c) autoregressive DLM contextual embeddings capture the neural representation of context-specific word meaning better than arbitrary or static semantic embeddings. Together, our findings suggest that autoregressive DLMs provide a novel and biologically feasible computational framework for studying the neural basis of language.

neuroscience↗

bioRxiv2020

Cortical network underlying speech production during delayed auditory feedback

Hearing ones 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 estimate and subsequent motor commands to produce intended speech. We were able to localize these neural markers using electrocorticographic recordings from neurosurgical subjects during a delayed auditory feedback (DAF) paradigm. In this task, subjects 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 two regions. Critically, response enhancement in dPreCG occurred only when subjects profoundly slowed down their speech 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 updating the internal speech estimates to maintain fluency as well as coordinating the efference copy and auditory error signals during speech production.

neuroscience↗

bioRxiv2020

Hierarchical integration across multiple timescales in human auditory cortex

To derive meaning from sound, the brain must integrate information across tens (e.g. phonemes) to hundreds (e.g. words) of milliseconds, but the neural computations that enable multiscale integration remain unclear. Prior evidence suggests that human auditory cortex analyzes sound using both generic acoustic features (e.g. spectrotemporal modulation) and category-specific computations, but how these putatively distinct computations integrate temporal information is unknown. To answer this question, we developed a novel method to estimate neural integration periods and applied the method to intracranial recordings from human epilepsy patients. We show that integration periods increase three-fold as one ascends the auditory cortical hierarchy. Moreover, we find that electrodes with short integration periods (~50-150 ms) respond selectively to spectrotemporal modulations, while electrodes with long integration periods (~200-300 ms) show prominent selectivity for sound categories such as speech and music. These findings reveal how multiscale temporal analysis organizes hierarchical computation in human auditory cortex.

neuroscience↗

bioRxiv2020

Spatiotemporal dynamics between interictal epileptiform discharges and ripples during associative memory processing

We describe the spatiotemporal course of cortical high-gamma activity (HGA), hippocampal ripple activity and interictal epileptiform discharges (IEDs) during an associative memory task in 15 epilepsy patients undergoing invasive electroencephalography. Successful encoding trials manifested significantly greater HGA in hippocampus and frontal regions. Successful cued recall trials manifested sustained HGA in hippocampus compared to failed responses. Hippocampal ripple rates were greater during successful encoding and retrieval trials. IEDs during encoding were associated with 15% decreased odds of remembering in hippocampus (95% CI 6-23%). Hippocampal IEDs during retrieval predicted 25% decreased odds of remembering (15-33%). Odds of remembering were reduced by 25-52% if IEDs occurred during the 500-2000 ms window of encoding or by 41% during retrieval. During encoding and retrieval, hippocampal IEDs were followed by a transient decrease in ripple rate. We hypothesize that IEDs impair associative memory in a regionally and temporally specific manner by decreasing physiologic hippocampal ripples necessary for effective encoding and recall. Because dynamic memory impairment arises from pathological IED events competing with physiological ripples, IEDs represent a promising therapeutic target for memory remediation in patients with epilepsy. SummaryHippocampal interictal epileptiform discharges in hippocampus acutely impair declarative memory, potentially by hijacking physiological processes essential for encoding and recall.

neuroscience↗

bioRxiv2020

Dual mechanisms of ictal high frequency oscillations in human rhythmic onset seizures

High frequency oscillations (HFOs) recorded from intracranial electrodes during epileptiform discharges are a proposed biomarker of epileptic brain tissue and may also be useful for seizure forecasting, with mixed results. Despite such potential for HFOs, there is limited investigation into the spatial context of HFOs and their relationship to simultaneously recorded neuronal activity. We sought to further understand the biophysical underpinnings of ictal HFOs using unit recordings in the human neocortex and mesial temporal lobe during rhythmic onset seizures. We compare features of ictal discharges in both the seizure core and penumbra (spatial seizure domains defined by multiunit activity patterns). We report differences in spectral features, unit-local field potential coupling, and information theoretic characteristics of HFOs before and after local seizure invasion. Furthermore, we tie these timing-related differences to spatial domains of seizures, showing that penumbral discharges are widely distributed and less useful for seizure localization.

physiology↗