Task-Specific Somatosensory Feedback via Cortical Stimulation in Humans

Abstract

Cortical stimulation through electrocorticographic (ECoG) electrodes is a potential method for providing sensory feedback in future prosthetic and rehabilitative applications. Here, we evaluate human subjects' ability to continuously modulate their motor behavior based on feedback from direct surface stimulation of the somatosensory cortex. Subjects wore a dataglove that measured their hand aperture position and received one of three stimuli over the hand sensory cortex based on their current hand position as compared to a target aperture position. Using cortical stimulation feedback, subjects adjusted their hand aperture to move towards the target aperture region. One subject was able to achieve accuracies and R² values well above chance (best performance: R² = 0.93; accuracy = 0.76/1). Performance dropped during the catch trial (same stimulus independent of the position) to below chance levels, suggesting that the subject had been using the varied sensory feedback to modulate their motor behavior. To our knowledge, this study represents one of the first demonstrations of using direct cortical surface stimulation of the human sensory cortex to perform a motor task, and is a first step towards developing closed-loop human sensorimotor brain-computer interfaces.

Fig. 1

Subject 2’s ECoG grid location. Left hemisphere implanted ECoG grid with the stimulating electrodes highlighted in white. The subject perceived an abstract sensation in the proximal and middle phalanges of his right middle finger following cortical stimulation over these electrodes.

Fig. 2

Traces of Subject 2’s hand aperture position relative to the aperture target thresholds with corresponding stimulation current amplitudes (a: Trial 9, b: Trial 13). Stimulation pulses were biphasic, but due to the time scale only the 200 ms stimulation trains are visible not the individual pulses (Stim 1 = 2.0 mA, Stim 2 = 2.4 mA, ITI Trial 9 = 800/800 and ITI Trial 13 = 800/400 for Stim 1/Stim 2, Table 3). Subjects’ aperture values could move outside of the 0 to 1 range if they made hand movements that were outside of the range used during the normalization period (Section 2.4). Subjects were instructed to start each run with their hand open in order to begin in the no-stimulation region (Table 1, Case A). Subject 2 sometimes overshot the target boundaries, but responded to error feedback (Case A, no stimulation; or, Case C, higher-intensity stimulation) by changing his direction of motion. a) Subject 2 was able to follow the target pathway and stay in the target boundaries with a high performance of: accuracy = 0.6145, R² = 0.8194. b) Subject 2 had trouble finding the target region at the beginning of the trial, resulting in lower performance values of: accuracy = 0.4023, R² = 0.1001.

Fig. 3

Subject 2’s accuracy levels as a measure of performance. Accuracy was calculated as (samples inside target range)/(total samples) while chance levels were determined with 1,000 simulated random walks. Mean chance accuracy values with error bars for the standard deviation are displayed. The subject’s accuracy is above chance level for 11 of the 13 non-catch trials. During the setup trial the subject had trouble mapping the cortical stimulation to the necessary motor response, but used the following 3 training trials with concurrent visual and stimulation feedback (shaded, trials 2–4) to explore the state space and learn to use the feedback. His accuracy dropped to below chance levels during the catch trial (same stimulation feedback regardless of the state) suggesting that he was relying on the cortical stimulation to achieve a high performance. Table 3 lists the stimulation amplitudes and ITIs for each trial. *Trials 13 and 14 used a shorter ITI for Stim 2 than the previous trials.

Fig. 4

Subject 2’s R² values as a measure of performance. Shaded trials 2–4 used concurrent visual and cortical stimulation feedback. Chance values were simulated with the random walks used for the accuracy chance calculations. Mean chance R² values with error bars for the standard deviation are displayed. The R² values follow a trend similar to the accuracy values (Fig. 3), and considered together the accuracy values and the R² values can illustrate the subject’s overall performance. In trials with high accuracies and high R² values, the subject slowly opened and closed his hand and remained relatively close to the target region even when he exited it. In trial 13, with a low R² value and higher accuracy, the subject deviated largely from the target region while searching for it (Fig. 2b), and then eventually found and followed the path increasing his accuracy but not his R² value. Again, Table 3 lists the stimulation amplitudes and ITIs for each trial. *Trials 13 and 14 used a shorter ITI for Stim 2 than the previous trials.