A roadmap for implanting microelectrode arrays to evoke tactile sensations through intracortical microstimulation.

Intracortical microstimulation (ICMS) is a method for restoring sensation to people with paralysis as part of a bidirectional brain-computer interface to restore upper limb function. Evoking tactile sensations of the hand through ICMS requires precise targeting of implanted electrodes. Here we describe the presurgical imaging procedures used to generate functional maps of the hand area of the somatosensory cortex and subsequent planning that guided the implantation of intracortical microelectrode arrays. In five participants with cervical spinal cord injury, across two study locations, this procedure successfully enabled ICMS-evoked sensations localized to at least the first four digits of the hand. The imaging and planning procedures developed through this clinical trial provide a roadmap for other brain-computer interface studies to ensure successful placement of stimulation electrodes.

Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex.

The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded - in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands - the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger's movement. Moreover, the indirect effects of S1 ICMS on M1 were 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 conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation.

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

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. 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.

A visual brain-computer interface as communication aid for patients with amyotrophic lateral sclerosis.

OBJECTIVE: Brain-Computer Interface (BCI) spellers that make use of code-modulated Visual Evoked Potentials (cVEP) may provide a fast and more accurate alternative to existing visual BCI spellers for patients with Amyotrophic Lateral Sclerosis (ALS). However, so far the cVEP speller has only been tested on healthy participants. METHODS: We assess the brain responses, BCI performance and user experience of the cVEP speller in 20 healthy participants and 10 ALS patients. All participants performed a cued and free spelling task, and a free selection of Yes/No answers. RESULTS: 27 out of 30 participants could perform the cued spelling task with an average accuracy of 79% for ALS patients, 88% for healthy older participants and 94% for healthy young participants. All 30 participants could answer Yes/No questions freely, with an average accuracy of around 90%. CONCLUSIONS: With ALS patients typing on average 10 characters per minute, the cVEP speller presented in this paper outperforms other visual BCI spellers. SIGNIFICANCE: These results support a general usability of cVEP signals for ALS patients, which may extend far beyond the tested speller to control e.g. an alarm, automatic door, or TV within a smart home.

Free Wally: Where motor intentions meet reason and consequence.

To investigate the neural preparation and awareness of an intention to act, neuroscientists typically examine spontaneous movements: self-paced flexions of the hand or foot. However, these movements may not present a straightforward case of intended action as they are performed in absence of reasons to act and without the evaluation of action consequences. Therefore, a common criticism of these studies is that they lack ecological validity, because the results do not generalize to the more societally relevant deliberate actions that we perform in daily life. We agree that research on intended action should include reason-based deliberate actions in order to be more relevant for debates about human agency and free will. Therefore, we have developed a computer game called "Free Wally", which invites players to perform deliberate actions to achieve a goal. Free Wally provides a controlled environment for studying deliberate intended action, by presenting information for deciding whether or not to act, what action to perform and when to perform it, incorporating all basic components of an ecologically valid intended act. As a first step to validate our setup, we compare this game to a second computer game that measures spontaneous actions in a traditional way. While playing either game, the timing of the experienced intentions to act is measured using a real-time probing method. Moreover, the neural preparation for action is measured in terms of the (lateralized) readiness potential and alpha/beta event-related desynchronization across the motor cortex. No differences were found between the games in these last stages of action preparation, suggesting that the Free Wally game can be used to study intended action. However, differences in earlier stages during intention formation are to be expected. With Free Wally as a tool, we hope to encourage further research into the formation and content of ecologically valid motor intentions.

Probing for Intentions: Why Clocks Do Not Provide the Only Measurement of Time.

Having an intention to act is commonly operationalized as the moment at which awareness of an urge or decision to act arises. Measuring this moment has been challenging due to the dependence on first-person reports of subjective experience rather than objective behavioral or neural measurements. Commonly, this challenge is met using (variants of) Libet's clock method. In 2008, Matsuhashi and Hallett published a novel probing strategy as an alternative to the clock method. We believe their probe method could provide a valuable addition to the clock method because: it measures the timing of an intention in real-time, it can be combined with additional (tactile, visual or auditory) stimuli to create a more ecologically valid experimental context, and it allows the measurement of the point of no return. Yet to this date, the probe method has not been applied widely - possibly due to concerns about the effects that the probes might have on the intention and/or action preparation processes. To address these concerns, a 2 × 2 within-subject design is tested. In this design, two variables are manipulated: (1) the requirement of an introspection report and (2) the presence of an auditory probe. Three observables are measured that provide information about the timing of an intention to act: (1) awareness reports of the subjective experience of having an intention, (2) neural preparatory activity for action, and (3) behavioral data of the performed actions. The presence of probes was found to speed up mean action times by roughly 300 ms, but did not alter the neural preparation for action. The requirement of an introspection report did influence brain signals: reducing the amplitude of the readiness potential and increasing the desynchronization in the alpha and beta bands over the motor cortex prior to action onset. By discussing the strengths and weaknesses of the probe method compared to the clock method, we hope to demonstrate its added value and promote its use in future research.

Detecting traces of consciousness in the process of intending to act.

An intention to act has different onsets when it is measured in different ways. When participants provide a self-initiated report on the onset of their awareness of intending to act, the report occurs around 150 ms prior to action. However, when the same participants are repeatedly asked about their awareness of intending at different points in time, the onset of intending is found up to 2 s prior to action. This 'probed' awareness has its onset around the same time as the brain starts preparing the act, as measured using EEG. First of all, this undermines straightforward interpretations about the temporal relation between unconscious brain states and conscious intentions and actions. Secondly, we suggest that these results present a problem for the view that intentions are mental states occurring at a single point in time. Instead, we suggest the results to support the interpretation of an intention to act as a multistage process developing over time. This process of intending seems to develop during the process of acting, leaving reportable traces in consciousness at certain points along the road.

Lost in time...: The search for intentions and Readiness Potentials.

In 1983 Libet et al. found that the Readiness Potential (RP) precedes the intention to act by 350ms and the actual movement by 500ms on average. Using our own replication study, we illustrate how seemingly innocuous technical details are actually crucially relevant to the debate surrounding the interpretation of Libet-style experiments. For instance, using one specific method for determining the RP onset actually led to a reversal of Libet's results (i.e., the intention preceded the RP onset) for one of the participants. Claims regarding the causal relation between RP and intention cannot be based on averages, but require individual, case by case analyses, which show no exceptions in the temporal relation between RP and intention. We conclude that, properly speaking, Libet-style results in themselves cannot yet be taken as proof for the type of conclusions that are often formulated regarding the non-existence of free will.