Search bioRxiv⌕ Search

Biology subjects

Downey, J. E.

Publications and source records attributed to Downey, J. E..

9 recordsLinked to original sources

Overlap in neural representations of coordinated wrist and finger movements in human motor cortex

Dexterous hand function underlies many essential human activities, from tool use to expression through gestures. Coordinated digit movements are enabled by the intricate musculature of the hand and forearm, which also imposes mechanical coupling between the digits and wrist, constraining their independent control. It remains unclear whether motor cortex inherits these constraints in its activity or encodes digit and wrist independently. To address this problem, we asked individuals with intracortical microelectrode arrays implanted in motor cortex to attempt flexion and extension of individual digits, either in isolation or in combination with attempted wrist movements. We could accurately decode which digit was moving based on cortical recordings, and channels selective for digit identity were arranged somatotopically across the recording arrays. Nevertheless, the activity during flexion or extension overlapped between digits, and movement direction of a given digit could be reliably inferred by a decoder trained on movements of other digits. This directional signal was largely invariant to the digits initial posture. The population axis describing digit movement direction was aligned with the axes associated with wrist flexion-extension or pronation-supination. This alignment persisted during simultaneous wrist and digit movements, which complicated efforts to control them individually. However, by decoding wrist and digit motion from activity orthogonal to the shared direction axis, a participant was able to achieve continuous control of virtual hand movements with improved speed and reduced unintended movements. Together, the results identify both a code for digit identity and a low-dimensional flexion-extension signal which is shared across the digits and wrist. This arrangement is consistent with muscle-like biomechanical constraints on motor cortical activity, which must be accounted for to improve coordinated BCI control.

neuroscience↗

Closed-loop error damping in human BCI using pre-error motor cortex activity

Intracortical brain-computer interfaces (BCIs) are used to decode motor intent from neural population activity; their main clinical application is to restore function for individuals with motor or communication deficits. However, when trying to reconstruct movement trajectories, such as in computer cursor control, even state-of-the-art decoders fall short of able-bodied performance during online BCI control. This calls for alternative approaches to improve the usability of motor BCIs. Here, we leveraged an error signal, i.e. a neural correlate of faulty motor control that can be detected from neural activity. By detecting this error signal in parallel to performing movement decoding, it is possible to perform error modulation, i.e. real-time error detection and correction during a closed-loop motor BCI task. We analyzed data from four individuals with upper limb impairment due to cervical spinal cord injury who each used an intracortical BCI to perform a continuous cursor control task with visual feedback. A classifier was trained to detect the error signal and was used to perform online error detection during BCI control to limit ongoing errors (defined as movement of the controller away from its target) without requiring any specific action from the participants. Our contribution is three-fold. First, we show that the error signal has a pre-error component. Cortical activity was already significantly modulated before the onset of the kinematically-defined error, theoretically allowing for earlier detection. Second, we show that error modulation significantly improves performance during online BCI control of cursor kinematics. Finally, we show that the error signal can be robustly leveraged across contexts, as error modulation improves performance in more complex motor tasks (involving for instance grasp and drag actions) or other environments without task-specific calibration. Overall, our results suggest that the error signal can be robustly disentangled from motor intent in cortical activity, and that even a simple linear classifier can enable error modulation in parallel to a continuous kinematic decoder, yielding more reliable and accurate BCI control.

neuroscience↗

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.

neuroscience↗

Neuronal firing rate diversity lowers the dimension of population covariability

Neuronal responses are very diverse, with specific stimuli or behaviors eliciting a range of activity across a neuronal population. These responses also show large and correlated trial-to-trial fluctuations that occupy a low-dimensional region in activity space. We link these two aspects of neuronal response in both feedforward and recurrent circuit models and derive the following relation: the more diverse the firing rates of neurons in a population, the lower the effective dimension of their trial-to-trial covariability. We test our prediction using simultaneously recorded neuronal populations from numerous brain areas in mice, non-human primates, and in the motor cortex of human participants. Finally, we show how diverse neural codes lead to better stimulus discrimination, and that when the brain is in a heightened state of processing responses are more diverse and have lower-dimensional fluctuations. In sum, we present an organizing principle of population response that is widely observed across the nervous system and acts to synergistically improve population representation.

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↗

Biomimetic multi-channel microstimulation of somatosensory cortex conveys high resolution force feedback for bionic hands

AO_SCPLOWBSTRACTC_SCPLOWManual interactions with objects are supported by tactile signals from the hand. This tactile feedback can be restored in brain-controlled bionic hands via intracortical microstimulation (ICMS) of somatosensory cortex (S1). In ICMS-based tactile feedback, contact force can be signaled by modulating the stimulation intensity based on the output of force sensors on the bionic hand, which in turn modulates the perceived magnitude of the sensation. In the present study, we gauged the dynamic range and precision of ICMS-based force feedback in three human participants implanted with arrays of microelectrodes in S1. To this end, we measured the increases in sensation magnitude resulting from increases in ICMS amplitude and participants ability to distinguish between different intensity levels. We then assessed whether we could improve the fidelity of this feedback by implementing "biomimetic" ICMS-trains, designed to evoke patterns of neuronal activity that more closely mimic those in natural touch, and by delivering ICMS through multiple channels at once. We found that multi-channel biomimetic ICMS gives rise to stronger and more distinguishable sensations than does its single-channel counterpart. Finally, we implemented biomimetic multi-channel feedback in a bionic hand and had the participant perform a compliance discrimination task. We found that biomimetic multi-channel tactile feedback yielded improved discrimination over its single-channel linear counterpart. We conclude that multi-channel biomimetic ICMS conveys finely graded force feedback that more closely approximates the sensitivity conferred by natural touch.

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↗

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↗