The effects of chronic intracortical microstimulation on neural tissue and fine motor behavior.

OBJECTIVE: One approach to conveying sensory feedback in neuroprostheses is to electrically stimulate sensory neurons in the cortex. For this approach to be viable, it is critical that intracortical microstimulation (ICMS) causes minimal damage to the brain. Here, we investigate the effects of chronic ICMS on the neuronal tissue across a variety of stimulation regimes in non-human primates. We also examine each animal's ability to use their hand--the cortical representation of which is targeted by the ICMS--as a further assay of possible neuronal damage. APPROACH: We implanted electrode arrays in the primary somatosensory cortex of three Rhesus macaques and delivered ICMS four hours per day, five days per week, for six months. Multiple regimes of ICMS were delivered to investigate the effects of stimulation parameters on the tissue and behavior. Parameters included current amplitude (10-100 µA), pulse train duration (1, 5 s), and duty cycle (1/1, 1/3). We then performed a range of histopathological assays on tissue near the tips of both stimulated and unstimulated electrodes to assess the effects of chronic ICMS on the tissue and their dependence on stimulation parameters. MAIN RESULTS: While the implantation and residence of the arrays in the cortical tissue did cause significant damage, chronic ICMS had no detectable additional effect; furthermore, the animals exhibited no impairments in fine motor control. SIGNIFICANCE: Chronic ICMS may be a viable means to convey sensory feedback in neuroprostheses as it does not cause significant damage to the stimulated tissue.

The effect of chronic intracortical microstimulation on the electrode-tissue interface.

OBJECTIVE: Somatosensation is critical for effective object manipulation, but current upper limb prostheses do not provide such feedback to the user. For individuals who require use of prosthetic limbs, this lack of feedback transforms a mundane task into one that requires extreme concentration and effort. Although vibrotactile motors and sensory substitution devices can be used to convey gross sensations, a direct neural interface is required to provide detailed and intuitive sensory feedback. The viability of intracortical microstimulation (ICMS) as a method to deliver feedback depends in part on the long-term reliability of implanted electrodes used to deliver the stimulation. The objective of the present study is to investigate the effects of chronic ICMS on the electrode-tissue interface. APPROACH: We stimulate the primary somatosensory cortex of three Rhesus macaques through chronically implanted electrodes for 4 h per day over a period of six months, with different electrodes subjected to different regimes of stimulation. We measure the impedance and voltage excursion as a function of time and of ICMS parameters. We also test the sensorimotor consequences of chronic ICMS by having animals grasp and manipulate small treats. MAIN RESULTS: We show that impedance and voltage excursion both decay with time but stabilize after 10-12 weeks. The magnitude of this decay is dependent on the amplitude of the ICMS and, to a lesser degree, the duration of individual pulse trains. Furthermore, chronic ICMS does not produce any deficits in fine motor control. SIGNIFICANCE: The results suggest that chronic ICMS has only a minor effect on the electrode-tissue interface and may thus be a viable means to convey sensory feedback in neuroprosthetics.

Natural scenes in tactile texture.

Sensory systems are designed to extract behaviorally relevant information from the environment. In seeking to understand a sensory system, it is important to understand the environment within which it operates. In the present study, we seek to characterize the natural scenes of tactile texture perception. During tactile exploration complex high-frequency vibrations are elicited in the fingertip skin, and these vibrations are thought to carry information about the surface texture of manipulated objects. How these texture-elicited vibrations depend on surface microgeometry and on the biomechanical properties of the fingertip skin itself remains to be elucidated. Here we record skin vibrations, using a laser-Doppler vibrometer, as various textured surfaces are scanned across the finger. We find that the frequency composition of elicited vibrations is texture specific and highly repeatable. In fact, textures can be classified with high accuracy on the basis of the vibrations they elicit in the skin. As might be expected, some aspects of surface microgeometry are directly reflected in the skin vibrations. However, texture vibrations are also determined in part by fingerprint geometry. This mechanism enhances textural features that are too small to be resolved spatially, given the limited spatial resolution of the neural signal. We conclude that it is impossible to understand the neural basis of texture perception without first characterizing the skin vibrations that drive neural responses, given the complex dependence of skin vibrations on both surface microgeometry and fingertip biomechanics.

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.

Spatial and temporal codes mediate the tactile perception of natural textures.

When we run our fingers over the surface of an object, we acquire information about its microgeometry and material properties. Texture information is widely believed to be conveyed in spatial patterns of activation evoked across one of three populations of cutaneous mechanoreceptive afferents that innervate the fingertips. Here, we record the responses evoked in individual cutaneous afferents in Rhesus macaques as we scan a diverse set of natural textures across their fingertips using a custom-made rotating drum stimulator. We show that a spatial mechanism can only account for the processing of coarse textures. Information about most natural textures, however, is conveyed through precise temporal spiking patterns in afferent responses, driven by high-frequency skin vibrations elicited during scanning. Furthermore, these texture-specific spiking patterns predictably dilate or contract in time with changes in scanning speed; the systematic effect of speed on neuronal activity suggests that it can be reversed to achieve perceptual constancy across speeds. The proposed temporal coding mechanism involves converting the fine spatial structure of the surface into a temporal spiking pattern, shaped in part by the mechanical properties of the skin, and ascribes an additional function to vibration-sensitive mechanoreceptive afferents. This temporal mechanism complements the spatial one and greatly extends the range of tangible textures. We show that a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture.

Multiplexing stimulus information through rate and temporal codes in primate somatosensory cortex.

Our ability to perceive and discriminate textures relies on the transduction and processing of complex, high-frequency vibrations elicited in the fingertip as it is scanned across a surface. How naturalistic vibrations, and by extension texture, are encoded in the responses of neurons in primary somatosensory cortex (S1) is unknown. Combining single unit recordings in awake macaques and perceptual judgments obtained from human subjects, we show that vibratory amplitude is encoded in the strength of the response evoked in S1 neurons. In contrast, the frequency composition of the vibrations, up to 800 Hz, is not encoded in neuronal firing rates, but rather in the phase-locked responses of a subpopulation of neurons. Moreover, analysis of perceptual judgments suggests that spike timing not only conveys stimulus information but also shapes tactile perception. We conclude that information about the amplitude and frequency of natural vibrations is multiplexed at different time scales in S1, and encoded in the rate and temporal patterning of the response, respectively.

The effect of surface wave propagation on neural responses to vibration in primate glabrous skin.

Because tactile perception relies on the response of large populations of receptors distributed across the skin, we seek to characterize how a mechanical deformation of the skin at one location affects the skin at another. To this end, we introduce a novel non-contact method to characterize the surface waves produced in the skin under a variety of stimulation conditions. Specifically, we deliver vibrations to the fingertip using a vibratory actuator and measure, using a laser Doppler vibrometer, the surface waves at different distances from the locus of stimulation. First, we show that a vibration applied to the fingertip travels at least the length of the finger and that the rate at which it decays is dependent on stimulus frequency. Furthermore, the resonant frequency of the skin matches the frequency at which a subpopulation of afferents, namely Pacinian afferents, is most sensitive. We show that this skin resonance can lead to a two-fold increase in the strength of the response of a simulated afferent population. Second, the rate at which vibrations propagate across the skin is dependent on the stimulus frequency and plateaus at 7 m/s. The resulting delay in neural activation across locations does not substantially blur the temporal patterning in simulated populations of afferents for frequencies less than 200 Hz, which has important implications about how vibratory frequency is encoded in the responses of somatosensory neurons. Third, we show that, despite the dependence of decay rate and propagation speed on frequency, the waveform of a complex vibration is well preserved as it travels across the skin. Our results suggest, then, that the propagation of surface waves promotes the encoding of spectrally complex vibrations as the entire neural population is exposed to essentially the same stimulus. We also discuss the implications of our results for biomechanical models of the skin.

Temporal frequency channels are linked across audition and touch.

Temporal frequency is a fundamental sensory dimension in audition and touch. In audition, analysis of temporal frequency is necessary for speech and music perception; in touch, the spectral analysis of vibratory signals has been implicated in texture perception and in sensing the environment through tools. Environmental oscillations impinging upon the ear are generally thought to be processed independently of oscillations impinging upon the skin. Here, we show that frequency channels are perceptually linked across audition and touch. In a series of psychophysical experiments, we demonstrate that auditory stimuli interfere with tactile frequency perception in a systematic manner. Specifically, performance on a tactile-frequency-discrimination task is impaired when an auditory distractor is presented with the tactile stimuli, but only if the frequencies of the auditory and tactile stimuli are similar. The frequency-dependent interference effect is observed whether the distractors are pure tones or band-pass noise, so an auditory percept of pitch is not required for the effect to be produced. Importantly, distractors that strongly impair frequency discrimination do not interfere with judgments of tactile intensity. This surprisingly specific crosstalk between different modalities reflects the importance of supramodal representations of fundamental sensory dimensions.

A dense array stimulator to generate arbitrary spatio-temporal tactile stimuli.

The generation and presentation of tactile stimuli presents a unique challenge. Unlike vision and audition, in which standard equipment such as monitors and audio systems can be used for most experiments, tactile stimuli and/or stimulators often have to be tailor-made for a given study. Here, we present a novel tactile stimulator designed to present arbitrary spatio-temporal stimuli to the skin. The stimulator consists of 400 pins, arrayed over a 1cm(2) area, each under independent computer control. The dense array allows for an unprecedented number of stimuli to be presented within an experimental session (e.g., up to 1200 stimuli per minute) and for stimuli to be generated adaptively. The stimulator can be used in a variety of modes and can deliver indented and scanned patterns as well as stimuli defined by mathematical spatio-temporal functions (e.g., drifting sinusoids). We describe the hardware and software of the system, and discuss previous and prospective applications.