Flexible regulation of representations on a drifting manifold enables long-term stable complex neuroprosthetic control.

The nervous system needs to balance the stability of neural representations with plasticity. It is unclear what is the representational stability of simple actions, particularly those that are well-rehearsed in humans, and how it changes in new contexts. Using an electrocorticography brain-computer interface (BCI), we found that the mesoscale manifold and relative representational distances for a repertoire of simple imagined movements were remarkably stable. Interestingly, however, the manifold's absolute location demonstrated day-to-day drift. Strikingly, representational statistics, especially variance, could be flexibly regulated to increase discernability during BCI control without somatotopic changes. Discernability strengthened with practice and was specific to the BCI, demonstrating remarkable contextual specificity. Accounting for drift, and leveraging the flexibility of representations, allowed neuroprosthetic control of a robotic arm and hand for over 7 months without recalibration. Our study offers insight into how electrocorticography can both track representational statistics across long periods and allow long-term complex neuroprosthetic control.

Sleep spindles, stress and PTSD: The state of the science and future directions.

Sleep spindles are a signature feature of non-REM (NREM) sleep, with demonstrated relationships to sleep maintenance and learning and memory. Because PTSD is characterized by disturbances in sleep maintenance and in stress learning and memory, there is now a growing interest in examining the role of sleep spindles in the neurobiology of PTSD. This review provides an overview of methods for measuring and detecting sleep spindles as they pertain to human PTSD and stress research, presents a critical review of early findings examining sleep spindles in PTSD and stress neurobiology, and proposes several directions for future research. In doing so, this review underscores the extensive heterogeneity in sleep spindle measurement and detection methods, the wide range of spindle features that may be and have been examined, the many persisting unknowns about the clinical and functional relevance of those features, and the problems considering PTSD as a homogeneous group in between-group comparisons. This review also highlights the progress that has been made in this field and underscores the strong rationale for ongoing work in this area.

Sleep Spindles Favor Emotion Regulation Over Memory Consolidation of Stressors in Posttraumatic Stress Disorder.

BACKGROUND: Posttraumatic stress disorder (PTSD) is a trauma-induced condition, characterized by intrusive memories and trauma-associated anxiety. Non-rapid eye movement (NREM) sleep spindles might play a crucial role in learning and consolidating declarative stressor information. However, sleep and possibly sleep spindles are also known to regulate anxiety, suggestive of a dual role for sleep spindles in the processing of stressors. Specifically, in individuals with high PTSD symptom burden, spindles might fail to regulate anxiety levels after exposure and instead might maladaptively consolidate stressor information. METHODS: To disentangle the role of spindles in declarative memory versus anxiety regulation after stressor exposure and to examine the role of PTSD in these processes, we measured nap sleep after a cohort of 45 trauma-exposed participants were exposed to laboratory stress. Participants (high vs. low PTSD symptoms) completed 2 visits: a stress visit involving exposure to negatively valent images before nap and a control visit. In both visits, sleep was monitored via electroencephalography. A stressor recall session occurred after the nap in the stress visit. RESULTS: Stage 2 NREM (NREM2) spindle rates were higher in stress versus control sleep, indicative of stress-induced changes in spindles. In participants with high PTSD symptoms, NREM2 spindle rates in stress sleep predicted poorer recall accuracy of stressor images relative to participants with low PTSD symptoms, while correlating with greater reduction in stressor-induced anxiety levels after sleep. CONCLUSIONS: Contrary to our expectations, although spindles are known to play a role in declarative memory processes, our findings highlight an important role for spindles in sleep-dependent anxiety regulation in PTSD.

Compartmentalized dynamics within a common multi-area mesoscale manifold represent a repertoire of human hand movements.

The human hand is unique in the animal kingdom for unparalleled dexterity, ranging from complex prehension to fine finger individuation. How does the brain represent such a diverse repertoire of movements? We evaluated mesoscale neural dynamics across the human "grasp network," using electrocorticography and dimensionality reduction methods, for a repertoire of hand movements. Strikingly, we found that the grasp network represented both finger and grasping movements alike. Specifically, the manifold characterizing the multi-areal neural covariance structure was preserved during all movements across this distributed network. In contrast, latent neural dynamics within this manifold were surprisingly specific to movement type. Aligning latent activity to kinematics further uncovered distinct submanifolds despite similarities in synergistic coupling of joints between movements. We thus find that despite preserved neural covariance at the distributed network level, mesoscale dynamics are compartmentalized into movement-specific submanifolds; this mesoscale organization may allow flexible switching between a repertoire of hand movements.

Emergence of perceptuomotor relationships during paleolithic stone toolmaking learning: intersections of observation and practice.

Stone toolmaking is a human motor skill which provides the earliest archeological evidence motor skill and social learning. Intentionally shaping a stone into a functional tool relies on the interaction of action observation and practice to support motor skill acquisition. The emergence of adaptive and efficient visuomotor processes during motor learning of such a novel motor skill requiring complex semantic understanding, like stone toolmaking, is not understood. Through the examination of eye movements and motor skill, the current study sought to evaluate the changes and relationship in perceptuomotor processes during motor learning and performance over 90 h of training. Participants' gaze and motor performance were assessed before, during and following training. Gaze patterns reveal a transition from initially high gaze variability during initial observation to lower gaze variability after training. Perceptual changes were strongly associated with motor performance improvements suggesting a coupling of perceptual and motor processes during motor learning.

Flexible constraint hierarchy during the visual encoding of tool-object interactions.

Tools and objects are associated with numerous action possibilities that are reduced depending on the task-related internal and external constraints presented to the observer. Action hierarchies propose that goals represent higher levels of the hierarchy while kinematic patterns represent lower levels of the hierarchy. Prior work suggests that tool-object perception is heavily influenced by grasp and action context. The current study sought to evaluate whether the presence of action hierarchy can be perceptually identified using eye tracking during tool-object observation. We hypothesize that gaze patterns will reveal a perceptual hierarchy based on the observed task context and grasp constraints. Participants viewed tool-objects scenes with two types of constraints: task-context and grasp constraints. Task-context constraints consisted of correct (e.g., frying pan-spatula) and incorrect tool-object pairings (e.g., stapler-spatula). Grasp constraints involved modified tool orientations, which requires participants to understand how initially awkward grasp postures can help achieve the task. The visual scene contained three areas of interests (AOIs): the object, the functional tool-end (e.g., spoon handle) and the manipulative tool-end (e.g., spoon bowl). Results revealed two distinct processes based on stimuli constraints. Goal-oriented encoding, the attentional bias towards the object and manipulative tool-end, was demonstrated when grasp did not lead to meaningful tool-use. In images where grasp postures were critical to action performance, attentional bias was primarily between the object and functional tool-end, which suggests means-related encoding of the graspable properties of the object. This study expands from previous work and demonstrates a flexible constraint hierarchy depending on the observed task constraints.

Plug-and-play control of a brain-computer interface through neural map stabilization.

Brain-computer interfaces (BCIs) enable control of assistive devices in individuals with severe motor impairments. A limitation of BCIs that has hindered real-world adoption is poor long-term reliability and lengthy daily recalibration times. To develop methods that allow stable performance without recalibration, we used a 128-channel chronic electrocorticography (ECoG) implant in a paralyzed individual, which allowed stable monitoring of signals. We show that long-term closed-loop decoder adaptation, in which decoder weights are carried across sessions over multiple days, results in consolidation of a neural map and 'plug-and-play' control. In contrast, daily reinitialization led to degradation of performance with variable relearning. Consolidation also allowed the addition of control features over days, that is, long-term stacking of dimensions. Our results offer an approach for reliable, stable BCI control by leveraging the stability of ECoG interfaces and neural plasticity.

The Role of Attention and Saccades on Parietofrontal Encoding of Contextual and Grasp-specific Affordances of Tools: An ERP Study.

The ability to recognize a tool's affordances (how a spoon should be appropriately grasped and used), is vital for daily life. Prior research has identified parietofrontal circuits, including mirror neurons, to be critical in understanding affordances. However, parietofrontal action-encoding regions receive extensive visual input and are adjacent to parietofrontal attention control networks. It is unclear how eye movements and attention modulate parietofrontal encoding of affordances. To address this issue, scenes depicting tools in different use-contexts and grasp-postures were presented to healthy subjects across two experiments, with stimuli durations of 100 ms or 500 ms. The 100-ms experiment automatically restricted saccades and required covert attention, while the 500-ms experiment allowed overt attention. The two experiments elicited similar behavioral decisions on tool-use correctness and isolated the influence of attention on parietofrontal activity. Parietofrontal ERPs (P600) distinguishing tool-use contexts (e.g., spoon-yogurt vs. spoon-ball) were similar in both experiments. Conversely, parietofrontal ERPs distinguishing tool-grasps were characterized by posterior to frontal N130-N200 ERPs in the 100-ms experiment and by saccade-perturbed N130-N200 ERPs, frontal N400 and parietal P500 in the 500-ms experiment. Particularly, only overt gaze toward the hand-tool interaction engaged mirror neurons (frontal N400) when discerning grasps that manipulate but not functionally use a tool - (grasp bowl rather than stem of spoon). Results here detail the first human electrophysiological evidence on how attention selectively modulates multiple parietofrontal grasp-perception circuits, especially the mirror neuron system, while unaffecting parietofrontal encoding of tool-use contexts. These results are pertinent to neurophysiological models of affordances that typically neglect the role of attention in action perception.

Shaping Reality through Mental Rehearsal.

Previous research has shown that mental rehearsal can improve performance. A new study by Vyas et al. (2018) reveals that direct modulation of neural dynamics using a brain-computer interface can also modify physical movements. The study further demonstrates that "mental practice" and physical movements share a common neural subspace.

Effects of somatosensory electrical stimulation on motor function and cortical oscillations.

BACKGROUND: Few patients recover full hand dexterity after an acquired brain injury such as stroke. Repetitive somatosensory electrical stimulation (SES) is a promising method to promote recovery of hand function. However, studies using SES have largely focused on gross motor function; it remains unclear if it can modulate distal hand functions such as finger individuation. OBJECTIVE: The specific goal of this study was to monitor the effects of SES on individuation as well as on cortical oscillations measured using EEG, with the additional goal of identifying neurophysiological biomarkers. METHODS: Eight participants with a history of acquired brain injury and distal upper limb motor impairments received a single two-hour session of SES using transcutaneous electrical nerve stimulation. Pre- and post-intervention assessments consisted of the Action Research Arm Test (ARAT), finger fractionation, pinch force, and the modified Ashworth scale (MAS), along with resting-state EEG monitoring. RESULTS: SES was associated with significant improvements in ARAT, MAS and finger fractionation. Moreover, SES was associated with a decrease in low frequency (0.9-4 Hz delta) ipsilesional parietomotor EEG power. Interestingly, changes in ipsilesional motor theta (4.8-7.9 Hz) and alpha (8.8-11.7 Hz) power were significantly correlated with finger fractionation improvements when using a multivariate model. CONCLUSIONS: We show the positive effects of SES on finger individuation and identify cortical oscillations that may be important electrophysiological biomarkers of individual responsiveness to SES. These biomarkers can be potential targets when customizing SES parameters to individuals with hand dexterity deficits. TRIAL REGISTRATION: NCT03176550; retrospectively registered.

Context and hand posture modulate the neural dynamics of tool-object perception.

Prior research has linked visual perception of tools with plausible motor strategies. Thus, observing a tool activates the putative action-stream, including the left posterior parietal cortex. Observing a hand functionally grasping a tool involves the inferior frontal cortex. However, tool-use movements are performed in a contextual and grasp specific manner, rather than relative isolation. Our prior behavioral data has demonstrated that the context of tool-use (by pairing the tool with different objects) and varying hand grasp postures of the tool can interact to modulate subjects' reaction times while evaluating tool-object content. Specifically, perceptual judgment was delayed in the evaluation of functional tool-object pairings (Correct context) when the tool was non-functionally (Manipulative) grasped. Here, we hypothesized that this behavioral interference seen with the Manipulative posture would be due to increased and extended left parietofrontal activity possibly underlying motor simulations when resolving action conflict due to this particular grasp at time scales relevant to the behavioral data. Further, we hypothesized that this neural effect will be restricted to the Correct tool-object context wherein action affordances are at a maximum. 64-channel electroencephalography (EEG) was recorded from 16 right-handed subjects while viewing images depicting three classes of tool-object contexts: functionally Correct (e.g. coffee pot-coffee mug), functionally Incorrect (e.g. coffee pot-marker) and Spatial (coffee pot-milk). The Spatial context pairs a tool and object that would not functionally match, but may commonly appear in the same scene. These three contexts were modified by hand interaction: No Hand, Static Hand near the tool, Functional Hand posture and Manipulative Hand posture. The Manipulative posture is convenient for relocating a tool but does not afford a functional engagement of the tool on the target object. Subjects were instructed to visually assess whether the pictures displayed correct tool-object associations. EEG data was analyzed in time-voltage and time-frequency domains. Overall, Static Hand, Functional and Manipulative postures cause early activation (100-400ms post image onset) of parietofrontal areas, to varying intensity in each context, when compared to the No Hand control condition. However, when context is Correct, only the Manipulative Posture significantly induces extended neural responses, predominantly over right parietal and right frontal areas [400-600ms post image onset]. Significant power increase was observed in the theta band [4-8Hz] over the right frontal area, [0-500ms]. In addition, when context is Spatial, Manipulative posture alone significantly induces extended neural responses, over bilateral parietofrontal and left motor areas [400-600ms]. Significant power decrease occurred primarily in beta bands [12-16, 20-25Hz] over the aforementioned brain areas [400-600ms]. Here, we demonstrate that the neural processing of tool-object perception is sensitive to several factors. While both Functional and Manipulative postures in Correct context engage predominantly an early left parietofrontal circuit, the Manipulative posture alone extends the neural response and transitions to a late right parietofrontal network. This suggests engagement of a right neural system to evaluate action affordances when hand posture does not support action (Manipulative). Additionally, when tool-use context is ambiguous (Spatial context), there is increased bilateral parietofrontal activation and, extended neural response for the Manipulative posture. These results point to the existence of other networks evaluating tool-object associations when motoric affordances are not readily apparent and underlie corresponding delayed perceptual judgment in our prior behavioral data wherein Manipulative postures had exclusively interfered in judging tool-object content.

One hand, two objects: emergence of affordance in contexts.

Studies on affordances typically focus on single objects. We investigated whether affordances are modulated by the context, defined by the relation between two objects and a hand. Participants were presented with pictures displaying two manipulable objects linked by a functional (knife-butter), a spatial (knife-coffee mug), or by no relation. They responded by pressing a key whether the objects were related or not. To determine if observing other's actions and understanding their goals would facilitate judgments, a hand was: (a) displayed near the objects; (b) grasping an object to use it; (c) grasping an object to manipulate/move it; (d) no hand was displayed. RTs were faster when objects were functionally rather than spatially related. Manipulation postures were the slowest in the functional context and functional postures were inhibited in the spatial context, probably due to mismatch between the inferred goal and the context. The absence of this interaction with foot responses instead of hands in Experiment 2 suggests that effects are due to motor simulation rather than to associations between context and hand-postures.