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Rubin, D. B.

Publications and source records attributed to Rubin, D. B..

9 recordsLinked to original sources

Learning-related population dynamics in right and left dorsal premotor cortex during typing skill acquisition

Advances in intracortical brain-computer interface (BCI) technology have enabled increasingly sophisticated communication paradigms, including for decoding intended speech and touch typing. However, the methods by which intracortical neural population dynamics are engaged during practice-related skill acquisition in humans remain poorly understood. Here, we examined learning-related changes in neural activity during motor skill acquisition in a right-handed BCI clinical trial participant with tetraplegia, with intracortical microelectrode arrays placed in the bilateral dorsal precentral gyri (Brodmann area 6d), who learned how to type using a BCI-enabled typing interface. While decoder performance remained stable across sessions, typing speed improved with practice, indicating practice-related skill acquisition. Over weeks, low-dimensional neural population activity became progressively more compact, and this compaction was strongly associated with faster typing, independent of decoder accuracy. Although this compaction was observed bilaterally in 6d, firing-rate modulation and cross-session generalization were selectively enhanced in left 6d. Moreover, neural population changes across sessions were largely accounted for by canonical correlation analysis in right 6d, but only partially accounted for in left 6d. Together, these findings demonstrate that human intracortical neuro-motor skill acquisition related to intended typing engages shared bilateral population-level dynamics, with additional learning-related changes selectively expressed in dominant dorsal premotor cortex.

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Observation-Related Activity in Human Motor Cortex Increases with Effector Anthropomorphicity

Neurons in motor cortex can be engaged not only in motor execution but also during observation of movements performed by other anthropomorphic agents (i.e. humans or monkeys). However, it is unknown how motor cortical neurons respond during observation of the range of assistive or prosthetic devices controlled by people using intracortical brain-computer interfaces (iBCIs). We recorded single-unit activity in the precentral gyrus while iBCI users viewed grasp-like movements performed by a spectrum of virtual effectors that included human, robotic, and hand-like dot stimuli. We found a relationship between neural modulation and effector anthropomorphicity (i.e. human-likeness) that existed on an ensemble-wide and individual neuron level, suggesting that human motor cortex activity incrementally increases in response to the visually observed agents human-likeness. Both solicited and spontaneous feedback from the participant indicated a relationship between neural activity and subjective assessments of anthropomorphicity, revealing a powerful contribution of context on observation-induced activity in motor cortex. The activity of motor cortex remained similar during attempted hand movements while different effectors were being observed, suggesting that intuitive external device control via iBCIs may not be overtly affected by the anthropomorphicity of the effector. SIGNIFICANCE STATEMENTThe tendency for neurons in motor cortex to respond during movement observation has been proposed to underlie cognitive processes from motor learning and language development to empathy and theory of mind. Understanding how the motor cortex is engaged during observation of abstract and anthropomorphic agents informs our understanding of these processes and may guide development of neural prostheses which harness the activity of motor cortical neurons to restore lost neurologic function. Here we provide unique neuron-level evidence that human motor cortex activity is gradually modulated by how human-like an observed agent appears and moves. This finding advances our interpretation of "mirror" activity in the brain and could help guide the design of brain-controlled prostheses used by people with tetraplegia.

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Cross-brain transfer of high-performance intracortical speech and handwriting BCIs

Intracortical brain-computer interfaces (BCIs) that decode complex movements, such as handwriting and speech, can require substantial training data to achieve high performance. We investigated whether leveraging the neural activity recordings of previous users could reduce this initial data collection burden for new BCI users (an approach we call "cross-brain transfer"). Using intracortical recordings from five BrainGate2 clinical trial participants, we tested cross-brain transfer for both speech and handwriting neural decoders trained and evaluated on general, unconstrained corpora of spoken and written English. We found that cross-brain transfer improved decoding performance when training data from the target user was limited (< 200 sentences), and that dataset-specific input layers to the decoder were critical for combining data across users. Without trainable input layers, transfer failed and performed worse than training from scratch on target user data only. Finally, we measured the effectiveness of cross-brain transfer relative to training with (1) more data from the same user and (2) more electrode-permuted data from the same user, which simulates sampling from another brain with identical neural latent structure. In some cases (T16 speech, T12 handwriting), cross-brain transfer appeared as effective as additional permuted data from the same user, while in others (T12 speech, T15 speech) electrode-permuted data was more beneficial. Our results successfully demonstrate and characterize cross-brain transfer learning between multiple intracortical BCI users, for both speech and handwriting, using a general open-ended dataset not restricted to small sets of words or phrases. This work highlights a promising path towards addressing a key barrier to the clinical translation of BCIs, while clarifying when cross-brain transfer may be most beneficial and the decoder design choices needed to realize those gains.

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Decoding intended speech with an intracortical brain-computer interface in a person with longstanding anarthria and locked-in syndrome

Intracortical brain-computer interfaces (iBCIs) for decoding intended speech have provided individuals with ALS and severe dysarthria an intuitive method for high-throughput communication. These advances have been demonstrated in individuals who are still able to vocalize and move speech articulators. Here, we decoded intended speech from an individual with longstanding anarthria, locked-in syndrome, and ventilator dependence due to advanced symptoms of ALS. We found that phonemes, words, and higher-order language units could be decoded well above chance. While sentence decoding accuracy was below that of demonstrations in participants with dysarthria, we are able to attain an extensive characterization of the neural signals underlying speech in a person with locked-in syndrome and through our results identify several directions for future improvement. These include closed-loop speech imagery training and decoding linguistic (rather than phonemic) units from neural signals in middle precentral gyrus. Overall, these results demonstrate that speech decoding from motor cortex may be feasible in people with anarthria and ventilator dependence. For individuals with longstanding anarthria, a purely phoneme-based decoding approach may lack the accuracy necessary to support independent use as a primary means of communication; however, additional linguistic information embedded within neural signals may provide a route to augment the performance of speech decoders.

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A mosaic of whole-body representations in human motor cortex

Understanding how the body is represented in motor cortex is key to understanding how the brain controls movement. The precentral gyrus (PCG) has long been thought to contain largely distinct regions for the arm, leg and face (represented by the "motor homunculus"). However, mounting evidence has begun to reveal a more intermixed, interrelated and broadly tuned motor map. Here, we revisit the motor homunculus using microelectrode array recordings from 20 arrays that broadly sample PCG across 8 individuals, creating a comprehensive map of human motor cortex at single neuron resolution. We found whole-body representations throughout all sampled points of PCG, contradicting traditional leg/arm/face boundaries. We also found two speech-preferential areas with a broadly tuned, orofacial-dominant area in between them, previously unaccounted for by the homunculus. Throughout PCG, movement representations of the four limbs were interlinked, with homologous movements of different limbs (e.g., toe curl and hand close) having correlated representations. Our findings indicate that, while the classic homunculus aligns with each areas preferred body region at a coarse level, at a finer scale, PCG may be better described as a mosaic of functional zones, each with its own whole-body representation.

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Human co-ripples facilitate neuronal interactions between cortical locations.

Synchronous bursts of high frequency oscillations ( ripples) are hypothesized to contribute to binding by facilitating integration of neuronal firing across cortical locations. We tested this hypothesis using local field-potentials and single-unit firing from four 96-channel microelectrode arrays in supragranular cortex of 3 patients. Neurons in co-rippling locations showed increased short-latency co-firing, prediction of each-others firing, and co-participation in neural assemblies. Effects were similar for putative pyramidal and interneurons, during NREM sleep and waking, in temporal and Rolandic cortices, and at distances up to 16mm. Increased co-prediction during co-ripples was maintained when firing-rate changes were equated, and were strongly modulated by ripple phase. Co-ripple enhanced prediction is reciprocal, synergistic with local upstates, and further enhanced when multiple sites co-ripple. Together, these results support the hypothesis that trans-cortical co-ripples increase the integration of neuronal firing of neurons in different cortical locations, and do so in part through phase-modulation rather than unstructured activation.

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Resting-State Electroencephalography for Continuous, Passive Prediction of Coma Recovery After Acute Brain Injury

Accurately predicting emergence from disorders of consciousness (DoC) after acute brain injury can profoundly influence mortality, acute management, and rehabilitation planning. While recent advances in functional neuroimaging and stimulus-based EEG offer the potential to enrich shared decision-making, their procedural sophistication and expense limit widespread availability or repeated performance. We investigated continuous EEG (cEEG) within a passive, "resting-state" framework to provide continuously updated predictions of DoC recovery at 24-, 48-, and 72-hour prediction horizons. To develop robust, continuous prediction models from a large population of patients with acute brain injury (ABI), we leveraged a recently described pragmatic approach transforming Glasgow Coma Scale assessment sub-score combinations into frequently assessed DoC diagnoses: coma, vegetative state, minimally conscious state with or without language, and post-injury confusional or recovered states. We retrospectively identified consecutive patients undergoing cEEG following acute traumatic brain injury (TBI), subarachnoid hemorrhage (SAH), or intracerebral hemorrhage (ICH). Models continuously predicting DoC diagnosis for multiple prediction horizons were evaluated utilizing recent clinical assessments with or without cEEG information, which comprised a comprehensive EEG feature set of 288 time, frequency, and time-frequency characteristics computed from consecutive 5-minute EEG epochs, with 6 additional features capturing each EEG features temporal dynamics. Features were fed into a predictive model developed with cross-validation; the ordinal DoC diagnosis was discriminated using an ensemble of XGBoost binary classifiers. For 201 ABI patients (46 TBI, 140 SAH, 15 ICH patients comprising 27,280 cEEG-hours with concomitant clinical assessments), cEEG-augmented models accurately predicted the future DoC diagnosis at 24 hours (one-vs-rest AU-ROC, 92.4%; weighted-F1 84.1%), 48 hours (one-vs-rest AU-ROC=88%, weighted-F1=80%) and 72 hours (one-vs-rest AU-ROC=86.3%, weighted-F1=76.6%). Models were robust to utilizing different ordinal cut-points for the DoC prediction target and evaluating additional models derived from specific sub-populations using a confound-isolating cross-validation framework. The most robust features across evaluation configurations included Petrosian fractal dimension, relative power of high to low (gamma-beta to delta-alpha) EEG frequency spectra, energy within the 12-35 Hz frequency band in the short-time Fourier transform domain, and wavelet entropy. The cEEG-augmented model exceeded the performance of models using preceding clinical assessments, continuously predicting future DoC diagnosis with one-vs-rest AU-ROC in the range of 84.3-92.4% while utilizing approaches to limit overfitting. The proposed continuous, resting-state cEEG prediction method represents a promising tool to predict DoC emergence in ABI patients. Enabling these methods prospectively would represent a new paradigm of continuous prognostic monitoring for predicting coma recovery and assessing treatment response.

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A simple circuit model of visual cortex explains neural and behavioral aspects of attention

Selective visual attention modulates neural activity in the visual system in complex ways and leads to enhanced performance on difficult visual tasks. Here, we show that a simple circuit model, the stabilized supralinear network, gives a unified account of a wide variety of effects of attention on neural responses. We replicate results from studies of both feature and spatial attention, addressing findings in a variety of experimental paradigms on changes both in firing rates and in correlated neural variability. Finally, we expand this circuit model into an architecture that can perform visual tasks--a convolutional neural network--in order to show that these neural effects can enhance detection performance. This work provides the first unified mechanistic account of the effects of attention on neural and behavioral responses.

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Stabilized supralinear network dynamics account for stimulus-induced changes of noise variability in the cortex

Variability and correlations in cortical activity are ubiquitously modulated by stimuli. Correlated variability is quenched following stimulus onset across multiple cortical areas, suppressing low-frequency components of the LFP and of Vm-LFP coherence. Modulation of Fano factors and correlations in area MT is tuned for stimulus direction. What circuit mechanisms underly these behaviors? We show that a simple model circuit, the stochastic Stabilized Supralinear Network (SSN), robustly explains these results. Stimuli modulate variability by modifying two forms of effective connectivity between activity patterns that characterize excitatory-inhibitory (E/I) circuits. Increases in the strength with which activity patterns inhibit themselves reduce correlated variability, while increases in feedforward connections between patterns (transforming E/I imbalance into balanced fluctuations) increase variability. These results suggest an operating regime of cortical dynamics that involves fast fluctuations and fast responses to stimulus changes, unlike previous models of variability suppression through suppression of chaos or networks with multiple attractors.

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