Postural Representations of the Hand in the Primate Sensorimotor Cortex.

Manual dexterity requires proprioceptive feedback about the state of the hand. To date, study of the neural basis of proprioception in the cortex has focused primarily on reaching movements to the exclusion of hand-specific behaviors such as grasping. To fill this gap, we record both time-varying hand kinematics and neural activity evoked in somatosensory and motor cortices as monkeys grasp a variety of objects. We find that neurons in the somatosensory cortex, as well as in the motor cortex, preferentially track time-varying postures of multi-joint combinations spanning the entire hand. This contrasts with neural responses during reaching movements, which preferentially track time-varying movement kinematics of the arm, such as velocity and speed of the limb, rather than its time-varying postural configuration. These results suggest different representations of arm and hand movements suited to the different functional roles of these two effectors.

Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex.

Intracortical microstimulation (ICMS) is a powerful tool to investigate the functional role of neural circuits and may provide a means to restore sensation for patients for whom peripheral stimulation is not an option. In a series of psychophysical experiments with nonhuman primates, we investigate how stimulation parameters affect behavioral sensitivity to ICMS. Specifically, we deliver ICMS to primary somatosensory cortex through chronically implanted electrode arrays across a wide range of stimulation regimes. First, we investigate how the detectability of ICMS depends on stimulation parameters, including pulse width, frequency, amplitude, and pulse train duration. Then, we characterize the degree to which ICMS pulse trains that differ in amplitude lead to discriminable percepts across the range of perceptible and safe amplitudes. We also investigate how discriminability of pulse amplitude is modulated by other stimulation parameters-namely, frequency and duration. Perceptual judgments obtained across these various conditions will inform the design of stimulation regimes for neuroscience and neuroengineering applications.

Long-term stability of sensitivity to intracortical microstimulation of somatosensory cortex.

OBJECTIVE: The dexterous manipulation of objects depends heavily on somatosensory signals from the limb. The development of anthropomorphic robotic arms and of algorithms to decode intended movements from neuronal signals has stimulated the need to restore somatosensation for use in upper-limb neuroprostheses. Without touch and proprioception, patients have difficulty controlling prosthetic limbs to a level that justifies the required invasive surgery. Intracortical microstimulation (ICMS) through chronically implanted electrode arrays has the potential to provide rich and intuitive sensory feedback. This approach to sensory restoration requires, however, that the evoked sensations remain stable over time. APPROACH: To investigate the stability of ICMS-evoked sensations, we measured the ability of non-human primates to detect ICMS over experimental sessions that spanned years. MAIN RESULTS: We found that the performance of the animals remained highly stable over time, even when they were tested with electrodes that had experienced extensive stimulation. SIGNIFICANCE: Given the stability of the sensations that it evokes, ICMS may thus be a viable approach for sensory restoration.

Sensitivity to microstimulation of somatosensory cortex distributed over multiple electrodes.

Meaningful and repeatable tactile sensations can be evoked by electrically stimulating primary somatosensory cortex. Intracortical microstimulation (ICMS) may thus be a viable approach to restore the sense of touch in individuals who have lost it, for example tetraplegic patients. One of the potential limitations of this approach, however, is that high levels of current can damage the neuronal tissue if the resulting current densities are too high. The limited range of safe ICMS amplitudes thus limits the dynamic range of ICMS-evoked sensations. One way to get around this limitation would be to distribute the ICMS over multiple electrodes in the hopes of intensifying the resulting percept without increasing the current density experienced by the neuronal tissue. Here, we test whether stimulating through multiple electrodes is a viable solution to increase the dynamic range of ICMS-elicited sensations without increasing the peak current density. To this end, we compare the ability of non-human primates to detect ICMS delivered through one vs. multiple electrodes. We also compare their ability to discriminate pulse trains differing in amplitude when these are delivered through one or more electrodes. We find that increasing the number of electrodes through which ICMS is delivered only has a marginal effect on detectability or discriminability despite the fact that 2-4 times more current is delivered overall. Furthermore, the impact of multielectrode stimulation (or lack thereof) is found whether pulses are delivered synchronously or asynchronously, whether the leading phase of the pulses is cathodic or anodic, and regardless of the spatial configuration of the electrode groups.

Restoring tactile and proprioceptive sensation through a brain interface.

Somatosensation plays a critical role in the dexterous manipulation of objects, in emotional communication, and in the embodiment of our limbs. For upper-limb neuroprostheses to be adopted by prospective users, prosthetic limbs will thus need to provide sensory information about the position of the limb in space and about objects grasped in the hand. One approach to restoring touch and proprioception consists of electrically stimulating neurons in somatosensory cortex in the hopes of eliciting meaningful sensations to support the dexterous use of the hands, promote their embodiment, and perhaps even restore the affective dimension of touch. In this review, we discuss the importance of touch and proprioception in everyday life, then describe approaches to providing artificial somatosensory feedback through intracortical microstimulation (ICMS). We explore the importance of biomimicry--the elicitation of naturalistic patterns of neuronal activation--and that of adaptation--the brain's ability to adapt to novel sensory input, and argue that both biomimicry and adaptation will play a critical role in the artificial restoration of somatosensation. We also propose that the documented re-organization that occurs after injury does not pose a significant obstacle to brain interfaces. While still at an early stage of development, sensory restoration is a critical step in transitioning upper-limb neuroprostheses from the laboratory to the clinic.

Restoring the sense of touch with a prosthetic hand through a brain interface.

Our ability to manipulate objects dexterously relies fundamentally on sensory signals originating from the hand. To restore motor function with upper-limb neuroprostheses requires that somatosensory feedback be provided to the tetraplegic patient or amputee. Given the complexity of state-of-the-art prosthetic limbs and, thus, the huge state space they can traverse, it is desirable to minimize the need for the patient to learn associations between events impinging on the limb and arbitrary sensations. Accordingly, we have developed approaches to intuitively convey sensory information that is critical for object manipulation--information about contact location, pressure, and timing--through intracortical microstimulation of primary somatosensory cortex. In experiments with nonhuman primates, we show that we can elicit percepts that are projected to a localized patch of skin and that track the pressure exerted on the skin. In a real-time application, we demonstrate that animals can perform a tactile discrimination task equally well whether mechanical stimuli are delivered to their native fingers or to a prosthetic one. Finally, we propose that the timing of contact events can be signaled through phasic intracortical microstimulation at the onset and offset of object contact that mimics the ubiquitous on and off responses observed in primary somatosensory cortex to complement slowly varying pressure-related feedback. We anticipate that the proposed biomimetic feedback will considerably increase the dexterity and embodiment of upper-limb neuroprostheses and will constitute an important step in restoring touch to individuals who have lost it.