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Biology subjects

Boninger, M. L.

Publications and source records attributed to Boninger, M. L..

8 recordsLinked to original sources

Distinct neural modes carry information about grasp force and phase in the sensorimotor cortex

Humans perform a variety of complex hand movements to manipulate objects, requiring precise control of changing forces. Understanding the role of sensorimotor cortex and the cortical dynamics underlying these actions is crucial for developing interventions that restore dexterous hand function after injury or disease. In this study, two individuals with tetraplegia resulting from cervical spinal cord injury attempted a series of isometric grasps. Neural activity was recorded from the motor and somatosensory cortices using intracortical microelectrode arrays while participants attempted to exert a static force or to ramp force up and down. Despite their inability to execute movement, and with limited afferent input, the spiking activity in motor and somatosensory cortex was modulated with the task. Within the neural response we identified independent neural modes - distinct patterns of population-level neural activity - that were informative about both the timing and magnitude of the force. Moreover, distinct neural modes were observed during static and dynamic grasping conditions, suggesting independent control schemes for maintaining and changing forces. These modes were related to phases of the task, including the onset, offset, holding periods, as well as phases of increasing and decreasing force. These results will inform the design of intracortical brain-computer interface (iBCI) systems that can leverage these naturally occurring patterns of grasp and force control to restore dexterous hand function. Significance StatementRestoring dexterous hand function after injury remains a major challenge, partly due to an incomplete understanding of the cortical dynamics underlying grasping and force control. In this study, we investigated neural activity within the motor and somatosensory cortices of individuals with tetraplegia attempting to perform grasps to different target forces with varying temporal profiles. We identified distinct neural modes modulated during specific phases of grasp that encode force information throughout the task. These findings suggest that brain-computer interfaces could leverage these native neural modes to restore grasping and force modulation.

neuroscience↗

A Generalist Intracortical Motor Decoder

Mapping the relationship between neural activity and motor behavior is a central aim of sensori-motor neuroscience and neurotechnology. While most progress to this end has relied on restricting complexity, the advent of foundation models instead proposes integrating a breadth of data as an alternate avenue for broadly advancing downstream modeling. We quantify this premise for motor decoding from intracortical microelectrode data, pretraining an autoregressive Transformer on 2000 hours of neural population spiking activity paired with diverse motor covariates from over 30 monkeys and humans. The resulting model is broadly useful, benefiting decoding on 8 downstream decoding tasks and generalizing to a variety of neural distribution shifts. However, we also highlight that scaling autoregressive Transformers seems unlikely to resolve limitations stemming from sensor variability and output stereotypy in neural datasets. Code: https://github.com/joel99/ndt3

neuroscience↗

How different immersive environments affect intracortical brain computer interfaces

AO_SCPLOWBSTRACTC_SCPLOWAs brain-computer interface (BCI) research advances, many new applications are being developed. Tasks can be performed in different environments, and whether a BCI user can switch environments seamlessly will influence the ultimate utility of a clinical device. Here we investigate the importance of the immersiveness of the virtual environment used to train BCI decoders on the resulting decoder and its generalizability between environments. Two participants who had intracortical electrodes implanted in their precentral gyrus used a BCI to control a virtual arm, either viewed immersively through virtual reality goggles or at a distance on a flat television monitor. Each participant performed better with a decoder trained and tested in the environment they had used the most prior to the study, one for each environment type. The neural tuning to the desired movement was minimally influenced by the immersiveness of the environment. Finally, in further testing with one of the participants, we found that decoders trained in one environment generalized well to the other environment, but the order in which the environments were experienced within a session mattered. Overall, experience with an environment was more influential on performance than the immersiveness of the environment, but BCI performance generalized well after accounting for experience.

neuroscience↗

Tessellation Of Artificial Touch Via Microstimulation Of Human Somatosensory Cortex

When we interact with objects, we rely on signals from the hand that convey information about the object and our interaction with it. A basic feature of these interactions, the locations of contacts between the hand and object, is often only available via the sense of touch. Information about locations of contact between a brain-controlled bionic hand and an object can be signaled via intracortical microstimulation (ICMS) of somatosensory cortex (S1), which evokes touch sensations that are localized to a specific patch of skin. To provide intuitive location information, tactile sensors on the robotic hand drive ICMS through electrodes that evoke sensations at skin locations matching sensor locations. This approach requires that ICMS-evoked sensations be focal, stable, and distributed over the hand. To systematically investigate the localization of ICMS-evoked sensations, we analyzed the projected fields (PFs) of ICMS-evoked sensations - their location and spatial extent - from reports obtained over multiple years from three participants implanted with microelectrode arrays in S1. First, we found that PFs vary widely in their size across electrodes, are highly stable within electrode, are distributed over large swaths of each participants hand, and increase in size as the amplitude or frequency of ICMS increases. Second, while PF locations match the locations of the receptive fields (RFs) of the neurons near the stimulating electrode, PFs tend to be subsumed by the corresponding RFs. Third, multi-channel stimulation gives rise to a PF that reflects the conjunction of the PFs of the component channels. By stimulating through electrodes with largely overlapping PFs, then, we can evoke a sensation that is experienced primarily at the intersection of the component PFs. To assess the functional consequence of this phenomenon, we implemented multi-channel ICMS-based feedback in a bionic hand and demonstrated that the resulting sensations are more localizable than are those evoked via single-channel ICMS.

neuroscience↗

Motor cortex retains and reorients neural dynamics during motor imagery

The most prominent role of motor cortex is generating patterns of neural activity that lead to movement, but it is also active when we simply imagine movements in the absence of actual motor output. Despite decades of behavioral and imaging studies, it is unknown how the specific activity patterns and temporal dynamics within motor cortex during covert motor imagery relate to those during motor execution. Here we recorded intracortical activity from the motor cortex of two people with residual wrist function following incomplete spinal cord injury as they performed both actual and imagined isometric wrist extensions. We found that we could decompose the population-level activity into orthogonal subspaces such that one set of components was similarly active during both action and imagery, and others were only active during a single task type--action or imagery. Although they inhabited orthogonal neural dimensions, the action-unique and imagery-unique subspaces contained a strikingly similar set of dynamical features. Our results suggest that during motor imagery, motor cortex maintains the same overall population dynamics as during execution by recreating the missing components related to motor output and/or feedback within a unique imagery-only subspace.

neuroscience↗

Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex

AO_SCPLOWBSTRACTC_SCPLOWMotor (M1) and somatosensory (S1) cortex play a critical role in motor control but the nature of the signaling between these structures is not known. To fill this gap, we recorded - in three human participants whose hands were paralyzed as a result of a spinal cord injury - the responses evoked in the hand and arm representations of primary motor cortex (M1) while we delivered ICMS to the somatosensory cortex (S1). We found that ICMS of S1 activated some M1 neurons at short, fixed latencies, locked to each pulse in a manner consistent with monosynaptic activation. However, most of the changes in M1 firing rates were much more variable in time, suggesting a more indirect effect of the stimulation. The spatial pattern of M1 activation varied systematically depending on the stimulating electrode: S1 electrodes that elicited percepts at a given hand location tended to activate M1 neurons with movement fields at the same location. However, the indirect effects of S1 ICMS on M1 were strongly context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS was used to convey tactile feedback about object interactions. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption could be minimized with biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, reduces sustained stimulation, and has been shown to convey useful contact-related information. SO_SCPLOWIGNIFICANCEC_SCPLOWMotor (M1) and somatosensory (S1) cortex play a critical role in motor control but the nature of the signaling between these structures is not known. To fill this gap, we recorded from M1 while delivering intracortical microstimulation (ICMS) to S1 of three human participants, whose hands were paralyzed by spinal cord injury. We found that ICMS activates M1 and that the motor fields of activated M1 neurons match the sensory fields of the stimulated S1 electrodes. These findings have important implications for using ICMS to convey tactile feedback for brain-controlled bionic hands. Indeed, the ICMS-evoked M1 activity worsens control of the hand. Fortunately, this effect is minimized by using biomimetic tactile feedback, which emphasizes contact transients and reduces sustained ICMS.

neuroscience↗

The effect of wrist posture on extrinsic finger muscle activity during single joint movements

Wrist posture impacts the muscle lengths and moment arms of the extrinsic finger muscles that cross the wrist. As a result, the electromyographic (EMG) activity associated with digit movement at different wrist postures may also change. Therefore, we sought to quantify the posture-dependence of extrinsic finger muscle activity. Fine-wire bipolar electrodes were inserted in the extrinsic hand muscles of able-bodied subjects to record EMG activity during wrist and finger movements in various postures. EMG activity of all the recorded finger muscles were significantly different (p<.05, ANOVA) when performing the same movement in five different wrist postures. EMG activity varied by up to 70%, with the highest levels of activity observed in finger extensors when the wrist was extended. Similarly, finger flexors were most active when the wrist was flexed. For the finger flexors, EMG variations with wrist posture were most prominent for index finger muscles, while the EMG activity of all finger extensor muscles were similarly modulated. The extrinsic finger muscles also showed significant activity during wrist movements with the digits held still regardless of finger posture, suggesting that they may play a role in generating torque during wrist movements. Finally, we developed a pair of generalized classifiers that show that finger muscle EMG can be used to predict wrist posture. These results may impact the design of biomimetic control algorithms for myoelectric prosthetic hands, but further work in transradial amputees is necessary to determine whether this phenomenon persists after amputation.

bioengineering↗

Restored tactile sensation improves neuroprosthetic arm control

Summary paragraphThe sense of touch is critical for skillful hand control1-3, but is largely missing for people who use prosthetic devices. Instead, prosthesis users rely heavily on visual feedback, even though state transitions that are necessary to skillfully interact with objects, such as object contact, are relayed more precisely through tactile feedback4-6. Here we show that restoring tactile sensory feedback, through intracortical microstimulation of the somatosensory cortex7, enables a person with a bidirectional intracortical brain-computer interface to improve their performance on functional object transport tasks completed with a neurally-controlled prosthetic limb. The participant had full visual feedback and had practiced the task for approximately two years prior to these experiments. Nevertheless, successful trial times on a commonly used clinical upper limb assessment task were reduced from a median time of 20.9 s (13.1 - 40.5 s interquartile range) to 10.2 s (5.4 - 18.1 s interquartile range) when vision was supplemented with microstimulation-evoked cutaneous percepts that were referred to different fingers and were graded in intensity based on real-time prosthesis contact forces. Faster completion times were primarily due to a reduction in the amount of time spent attempting to grasp objects. These results demonstrate the importance of tactile sensations in upper-limb control and the utility of creating bidirectional brain-computer interfaces to restore this stream of information using intracortical microstimulation.

clinical trials↗