Performing a motor task requires a feedback loop that informs the brain of success of each motor action. For sensory impaired this means brain computer interfaces must be bidirectional, requiring stimulation to close the loop.
In the previous blog posts we have been looking at BCI systems, whose function was to read signals from the brain. A bidirectional BCI, aims at both reading from and writing to the brain (or other parts of the nervous system). Thus, bidirectional interfaces aim at integrating both recording and relaying of information to and from the brain, in a single BCI system. Writing to the brain or other parts of the nervous system is done via stimulation for auditory, visual, tactile or proprioceptive feedback. For instance, several studies have shown that somatosensory feedback is an essential component for normal motor control. Already in the early 80s, a case study by Rothwell and colleagues showed that a person with chronic sensory impairment has severe difficulties in performing daily tasks such as holding a cup, buttoning a shirt or writing, but has no issues conducting instructed motor tasks in a lab setting [1]. This case study demonstrated that a fully formed motor plan (example buttoning a shirt), which can be considered a concatenation of simple motor actions, needs afferent feedback to inform concerned brain areas the success of each motor actions and also modify errors in execution before proceeding with the plan.
Figure : Example of a bidirectional (invasive) BCI where the neural activity from primary motor cortex is decoded for controlling the robotic arm, while also providing sensory feedback by (electrically) stimulating the primary somatosensory cortex. The figure is taken from [2]
Electrical stimulation
Electrical stimulation is commonly used to provide feedback and evoke sensation in the cortex and this can be achieved by placing electrodes on the surface of the brain – cortical surface stimulation or penetrating the surface of the brain – intracortical microstimulation.
Cortical surface stimulation
ECoG grids, which are most commonly implanted in patients suffering from intractable epilepsy, have been typically used to achieve cortical surface stimulation. These electrodes have a diameter of 4-5 mm and are typically 1 cm apart (distance between two electrode centers). ECoG stimulation has been routinely used to map the areas of eloquent cortex prior to surgical resection in such epilepsy patients. Stimulation studies using ECoG have been performed as part of monitoring studies in epileptic patients and it has been reported that cortical surface stimulation generates tingling or electrical feelings and in some cases the feeling is more natural (e.g. feeling of movement or light tapping). The location where such sensations are evoked depends on the location of the stimulated electrode and focal as well as sensations covering large areas have been reported.
See related post Stimulus, Sensation and Localization in the Cortex
With regard to bidirectional BCI applications, ownership over artificial limb has been reported in a study by Collins and colleagues [3]. The electrical stimulation was delivered to the hand section of the somatosensory cortex in synchrony with touches applied to a rubber hand. The study also reported that the feeling of ownership disappeared when the stimulation was delivered asynchronously (i.e. without the visual stimulus of touches ) or to other parts of the somatosensory cortex representing a body part other than the hand. It has also been shown that the intensity of the evoked sensation is highly dependent on the frequency, amplitude and pulse duration of the stimulation. Also, it has been reported that adjacent ECoG electrodes tend to evoke sensations from the same body part and stimulation of ECoG electrodes that were separated by at least one intermediate electrode could evoke sensations that were spatially distinct.
Overall, cortical surface stimulation using ECoG electrodes has shown to be useful for implementing bidirectional BCI. However, the performance is dependent on the electrode location as well as the distance between electrodes.
Intracortical microstimulation
Compared to ECoG stimulation, intracortical microstimulation is a much more invasive procedure, but has clear advantages over ECoG stimulation in terms of the electrode size and proximity to the target neurons thus requiring smaller stimulation currents. Also, the stimulation is more specific, as a smaller volume of neural tissue is stimulated compared to using large ECoG electrodes. This feature is particularly important for e.g. in restoring somatosensory capabilities of individual digits or even components of the digits [2].
It has been shown that intracortical microstimulation of the somatosensory cortex can provide sensory feedback, for example texture of objects in virtual space in non-human primates [4]. However with studies using non-human primates, it is not possible to measure the perceptual quality of the stimuli (i.e., non-human primates cannot ‘describe’ what the stimulation ‘feels’ like!). In one of the first studies to use intracortical stimulation in humans, Flesher and colleagues [5] showed that stimulating the hand area of somatosensory cortex with intracortical electrodes to evoke tactile sensations from the hand of a person with upper limb paralysis resulting from a spinal cord injury (See Figure 2). Another recent study has shown that using intracortical microstimulation tactile sensations can be evoked , thus providing grasp force feedback in patients with spinal cord injury [6]. Thus, intracortical microstimulation is a promising avenue for bidirectional BCI. However, it is more invasive than ECoG and has limited spatial coverage. This results in a trade off between the sensations focality and the range over which these sensations can be generated.
Figure 3. The colored areas of the hand represent the areas of perceived sensation by the subject when stimulated. The correspondence between the electrodes and the colored areas of the hand agree well with the known somatotopy of somatosensory cortex. Figure taken from Flesher and colleagues [5].
In addition to stimulating the central nervous system (either with ECoG or intracortical electrodes), stimulation of the peripheral nervous system has also been explored in bidirectional BCI. This works for users who still have intact spinal cord, for example amputees and peripheral stimulation has been used to evoke somatosensory percepts in such populations. For example, stimulation of the peripheral nervous system has been used to produce graded sensations of touch of their phantom hands as a feedback to their prosthetic arm using longitudinal intrafascicular electrodes [7]. Raspopovic and colleagues showed that an amputee could control prosthetic hand and receive somatosensory feedback using transverse intrafascicular electrodes [8].
The main advantage of peripheral interfaces is that it can activate the sensory system at more distal locations where the signals are less complex and more deterministic compared to signals acquired from the brain [2]
Disadvantages of electrical stimulation
Electrical stimulation for birectional BCI has shown great promise, but has certain disadvantages and challenges. These include – 1) unpredictable pathways of the current pulses delivered, 2) large stimulation artifacts that pose challenges in simultaneously decoding and providing feedback, 3) non-specificity due to limited spatial resolution. 4) Due to the design limitation of the electrodes, implantation can only be done in areas that are easily accessible on the brain surface, such as the human somatosensory cortex. Accessing deeper brain structures or regions of sulcus with these electrodes is still a challenge.
In the next blogpost we will look at optical stimulation techniques that overcome some of these challenges.
References
- Rothwell JC, Traub MM, Day BL et al. (1982). Manual motor performance in a deafferented man. Brain 105 (3): 515–542.
- Hughes, Christopher, et al. Bidirectional brain-computer interfaces. Handbook of clinical neurology. Vol. 168. Elsevier, 2020. 163-181.
- Collins, Kelly L., et al. Ownership of an artificial limb induced by electrical brain stimulation. Proceedings of the National Academy of Sciences 114.1 (2017): 166-171.
- O’Doherty, Joseph E., et al. Active tactile exploration using a brain-machine-brain interface. Nature 479.7372 (2011): 228-231.
- Flesher, Sharlene N., et al. Intracortical microstimulation of human somatosensory cortex. Science translational medicine 8.361 (2016).
- Quick, Kristin M., et al. Intracortical Microstimulation Feedback Improves Grasp Force Accuracy in a Human Using a Brain-Computer Interface. 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC). IEEE, 2020.
- Navarro, Xavier, et al. A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems. Journal of the Peripheral Nervous System 10.3 (2005): 229-258.
- Raspopovic, Stanisa, et al. “Restoring natural sensory feedback in real-time bidirectional hand prostheses.” Science translational medicine 6.222 (2014)
