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.is an important tool to investigate the functional role of neural circuits (1, 2). In a famous example, microstimulation of neurons in the middle temporal area was found to bias the perceived direction of visual motion stimuli, causally implicating these neurons in the computation of visual motion direction (3). Experiments with ICMS of somatosensory cortex showed that changing the frequency of stimulation elicited discriminable percepts, demonstrating that temporal patterning of cortical responses has perceptual correlates (4). Building on the success of these and other studies, ICMS has been proposed as an approach to restore perception in individuals who have lost it, for example in visual neuroprostheses for the blind (5, 6) or somatosensory neuroprostheses for tetraplegic patients (7-11). In the present study, we sought to characterize the psychometric properties of ICMS delivered to primary somatosensory cortex (S1) across a wide range of stimulation regimes. In psychophysical experiments with Rhesus macaques, we first measured the detectability of ICMS pulse trains and assessed its dependence on a variety of stimulation parameters. We then measured the degree to which animals could discriminate pairs of ICMS pulse trains that differed in amplitude. In both the detection and discrimination experiments, ICMS parameters-amplitude, pulse width, pulse train duration, and pulse train frequency-spanned the range that is detectable and has been typically deemed safe (12-14). Results from the present experiments will inform the design of future studies involving ICMS as well as the development of sensory encoding algorithms for neuroprostheses. ResultsWe trained two monkeys to perform two variants of a twoalternative forced-choice (2AFC) task: a detection task and a discrimination task. In both tasks, the animal was seated in front of a computer monitor that conveyed information about the trial...

A hallmark of tactile texture exploration is that it involves movement between skin and surface. When we scan a surface, small texture-specific vibrations are produced in the skin, and specialized cutaneous mechanoreceptors convert these vibrations into highly repeatable, precise, and informative temporal spiking patterns in tactile afferents. Both texture-elicited vibrations and afferent responses are highly dependent on exploratory kinematics, however; indeed, these dilate or contract systematically with decreases or increases in scanning speed, respectively. These profound changes in the peripheral response that accompany changes in scanning speed and other parameters of texture scanning raise the question as to whether exploratory behaviors change depending on what surface is explored or what information is sought about that surface. To address this question, we measure and analyze the kinematics as subjects explore textured surfaces to evaluate different types of texture information, namely the textures' roughness, hardness, and slipperiness. We find that the exploratory movements are dependent both on the perceptual task, as has been previously shown, but also on the texture that is scanned. We discuss the implications of our findings regarding the neural coding and perception of texture.

Manual interactions with objects require precise and rapid feedback about contact events. These tactile signals are integrated with motor plans throughout the neuraxis to achieve dexterous object manipulation. To better understand the role of somatosensory cortex in interactions with objects, we measured, using chronically implanted arrays of electrodes, the responses of populations of somatosensory neurons to skin indentations designed to simulate the initiation, maintenance, and termination of contact with an object. First, we find that the responses of somatosensory neurons to contact onset and offset dwarf their responses to maintenance of contact. Second, we show that these responses rapidly and reliably encode features of the simulated contact events—their timing, location, and strength—and can account for the animals’ performance in an amplitude discrimination task. Third, we demonstrate that the spatiotemporal dynamics of the population response in cortex mirror those of the population response in the nerves. We conclude that the responses of populations of somatosensory neurons are well suited to encode contact transients and are consistent with a role of somatosensory cortex in signaling transitions between task subgoals.

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.

Given the stability of the sensations that it evokes, ICMS may thus be a viable approach for sensory restoration.

Manual 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 participant's 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. We conclude that multi-channel biomimetic ICMS conveys finely graded force feedback that more closely approximates the sensitivity conferred by natural touch.

Intracortical microstimulation (ICMS) of somatosensory cortex evokes vivid tactile sensations and can be used to convey sensory feedback in brain-controlled bionic hands. Changes in ICMS frequency result in discriminable percepts, but the effects of frequency have only been investigated over a narrow range of low frequencies, spanning only a small fraction of that relevant for neuroprosthetics. Furthermore, the sensory correlates of changes in ICMS frequency remain to be elucidated. 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 reduce the animals' reliance on magnitude in making frequency judgments. We found that animals could discriminate ICMS frequency up to about 200 Hz but that the sensory correlates of frequency were highly electrode dependent. We discuss the implications of our findings for neural coding and brain-machine interfaces.

Objective.-Touch and proprioception are essential to motor function as shown by the movement deficits that result from the loss of these senses, e.g., due to neuropathy of sensory nerves. To achieve a high-performance brain-controlled prosthetic arm/hand thus requires the restoration of somatosensation, perhaps through intracortical microstimulation (ICMS) of somatosensory cortex (S1). The challenge is to generate patterns of neuronal activation that evoke interpretable percepts. We present a framework to design optimal spatiotemporal patterns of ICMS that evoke naturalistic patterns of neuronal activity and demonstrate performance superior to four previous approaches.Approach.-We recorded multiunit activity from S1 during a center-out reach task (from proprioceptive neurons in Brodmann's area 2) and during application of skin indentations (from cutaneous neurons in Brodmann's area 1). We implemented a computational model of a cortical hypercolumn and used a genetic algorithm to design spatiotemporal patterns of ICMS (STIM) that evoked patterns of model neuron activity that mimicked their experimentally-measured