The science and engineering behind sensitized brain-controlled bionic hands.

Advances in our understanding of brain function, along with the development of neural interfaces that allow for the monitoring and activation of neurons, have paved the way for brain-machine interfaces (BMIs), which harness neural signals to reanimate the limbs via electrical activation of the muscles or to control extracorporeal devices, thereby bypassing the muscles and senses altogether. BMIs consist of reading out motor intent from the neuronal responses monitored in motor regions of the brain and executing intended movements with bionic limbs, reanimated limbs, or exoskeletons. BMIs also allow for the restoration of the sense of touch by electrically activating neurons in somatosensory regions of the brain, thereby evoking vivid tactile sensations and conveying feedback about object interactions. In this review, we discuss the neural mechanisms of motor control and somatosensation in able-bodied individuals and describe approaches to use neuronal responses as control signals for movement restoration and to activate residual sensory pathways to restore touch. Although the focus of the review is on intracortical approaches, we also describe alternative signal sources for control and noninvasive strategies for sensory restoration.

Frequency Shapes the Quality of Tactile Percepts Evoked through Electrical Stimulation of the Nerves.

Electrical stimulation of the peripheral nerves of human participants provides a unique opportunity to study the neural determinants of perceptual quality using a causal manipulation. A major challenge in the study of neural coding of touch has been to isolate the role of spike timing-at the scale of milliseconds or tens of milliseconds-in shaping the sensory experience. In the present study, we address this question by systematically varying the pulse frequency (PF) of electrical stimulation pulse trains delivered to the peripheral nerves of seven participants with upper and lower extremity limb loss via chronically implanted neural interfaces. We find that increases in PF lead to systematic increases in perceived frequency, up to ∼50 Hz, at which point further changes in PF have little to no impact on sensory quality. Above this transition frequency, ratings of perceived frequency level off, the ability to discriminate changes in PF is abolished, and verbal descriptors selected to characterize the sensation change abruptly. We conclude that sensation quality is shaped by temporal patterns of neural activation, even if these patterns are imposed on a fixed neural population, but this temporal patterning can only be resolved up to ∼50 Hz. These findings highlight the importance of spike timing in shaping the quality of a sensation and will contribute to the development of encoding strategies for conveying touch feedback through bionic hands and feet.SIGNIFICANCE STATEMENT A major challenge in the study of neural coding of touch has been to understand how temporal patterns in neuronal responses shape the sensory experience. We address this question by varying the pulse frequency (PF) of electrical pulse trains delivered through implanted nerve interfaces in seven amputees. We concomitantly vary pulse width to separate the effect of changing PF on sensory quality from its effect on perceived magnitude. We find that increases in PF lead to increases in perceived frequency, a qualitative dimension, up to ∼50 Hz, beyond which changes in PF have little impact on quality. We conclude that temporal patterning in the neuronal response can shape quality and discuss the implications for restoring touch via neural interfaces.

The frequency of cortical microstimulation shapes artificial touch.

Intracortical microstimulation (ICMS) of the somatosensory cortex evokes vivid tactile sensations and can be used to convey sensory feedback from brain-controlled bionic hands. Changes in ICMS frequency lead to changes in the resulting sensation, but the discriminability of frequency has only been investigated over a narrow range of low frequencies. Furthermore, the sensory correlates of changes in ICMS frequency remain poorly understood. Specifically, it remains to be elucidated whether changes in frequency only modulate sensation magnitude-as do changes in amplitude-or whether they also modulate the quality of the sensation. To fill these gaps, we trained monkeys to discriminate the frequency of ICMS pulse trains over a wide range of frequencies (from 10 to 400 Hz). ICMS amplitude also varied across stimuli to dissociate sensation magnitude from ICMS frequency and ensure that animals could not make frequency judgments based on magnitude. We found that animals could consistently discriminate ICMS frequency up to ∼200 Hz but that the sensory correlates of frequency were highly electrode dependent: On some electrodes, changes in frequency were perceptually distinguishable from changes in amplitude-seemingly giving rise to a change in sensory quality; on others, they were not. We discuss the implications of our findings for neural coding and for brain-controlled bionic hands.

Case Studies in Neuroscience: Sensations elicited and discrimination ability from nerve cuff stimulation in an amputee over time.

The present case study details sensations elicited by electrical stimulation of peripheral nerve axons using an implanted nerve cuff electrode, in a participant with a transhumeral amputation. The participant uses an osseointegrated electromechanical interface, which enables skeletal attachment of the prosthesis and long-term, stable, bidirectional communication between the implanted electrodes and prosthetic arm. We focused on evoking somatosensory percepts, where we tracked and quantified the evolution of perceived sensations in the missing hand, which were evoked from electrical stimulation of the nerve, for over 2 yr. These sensations included small, pointlike areas of either vibration or pushing, to larger sensations over wider areas, indicating the recruitment of a few and many afferents, respectively. Furthermore, we used a two-alternative forced choice paradigm to measure the level of discrimination between trains of brief electrical stimuli, to gauge what the participant could reliably distinguish between. At best, the participant was able to distinguish a 0.5-Hz difference and on average acquired a 3.8-Hz just-noticeable difference at a more stringent psychophysical level. The current work shows the feasibility for long-term sensory feedback in prostheses, via electrical axonal stimulation, where small and relatively stable percepts were felt that may be used to deliver graded sensory feedback. This opens up opportunities for signaling feedback during movements (e.g., for precision grip), but also for conveying more complex cutaneous sensations, such as texture. NEW & NOTEWORTHY We demonstrate the long-term stability and generation of sensations from electrical peripheral nerve stimulation in an amputee, through an osseointegrated implant. We find that perceived tactilelike sensations could be generated for over 2 yr, in the missing hand. This is useful for prosthetic development and the implementation of feedback in artificial body parts.

Roughness encoding in human and biomimetic artificial touch: spatiotemporal frequency modulation and structural anisotropy of fingerprints.

The influence of fingerprints and their curvature in tactile sensing performance is investigated by comparative analysis of different design parameters in a biomimetic artificial fingertip, having straight or curved fingerprints. The strength in the encoding of the principal spatial period of ridged tactile stimuli (gratings) is evaluated by indenting and sliding the surfaces at controlled normal contact force and tangential sliding velocity, as a function of fingertip rotation along the indentation axis. Curved fingerprints guaranteed higher directional isotropy than straight fingerprints in the encoding of the principal frequency resulting from the ratio between the sliding velocity and the spatial periodicity of the grating. In parallel, human microneurography experiments were performed and a selection of results is included in this work in order to support the significance of the biorobotic study with the artificial tactile system.

Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans.

Restoration of touch after hand amputation is a desirable feature of ideal prostheses. Here, we show that texture discrimination can be artificially provided in human subjects by implementing a neuromorphic real-time mechano-neuro-transduction (MNT), which emulates to some extent the firing dynamics of SA1 cutaneous afferents. The MNT process was used to modulate the temporal pattern of electrical spikes delivered to the human median nerve via percutaneous microstimulation in four intact subjects and via implanted intrafascicular stimulation in one transradial amputee. Both approaches allowed the subjects to reliably discriminate spatial coarseness of surfaces as confirmed also by a hybrid neural model of the median nerve. Moreover, MNT-evoked EEG activity showed physiologically plausible responses that were superimposable in time and topography to the ones elicited by a natural mechanical tactile stimulation. These findings can open up novel opportunities for sensory restoration in the next generation of neuro-prosthetic hands.

Flexible three-axial force sensor for soft and highly sensitive artificial touch.

A soft tactile sensor able to detect both normal and tangential forces is fabricated with a simple method using conductive textile. Owing to the multi-layered architecture, the capacitive-based tactile sensor is highly sensitive (less than 10 mg and 8 µm, for minimal detectable weight and displacement, respectively) within a wide normal force range (potentially up to 27 N (400 kPa)) and natural touch-like tangential force ranges (from about 0.5 N to 1.8 N). Being flexible, soft, and low cost, this sensor represents an original approach in the emulation of natural touch.