Sequence of visual cortex stimulation affects phosphene brightness in blind subjects.

BACKGROUND: Visual cortical prostheses (VCP) could potentially benefit a majority of the blind population. Feasibility testing of these VCP opens new avenues to characterize stimulation of visual cortex in blind subjects. OBJECTIVE/HYPOTHESIS: To determine if sequential stimulation of visual cortex produces a perception bias in phosphene brightness. METHODS: We stimulated three blind subjects implanted with the Orion array with sequences of two and three electrodes and asked them to determine the brighter phosphene, using interval forced-choice paradigms. We selected a set of reference electrodes as the constant stimuli across sequences and compared across three different amplitude levels keeping all other stimulation parameters fixed across electrodes. RESULTS: For two subjects, we measured a significant increase in the probability of perceiving a lower-level amplitude just as bright or brighter than a higher-level amplitude when stimulated later in the sequence (p < 0.001, Wilcoxon rank sum test). The probability of reference electrodes selected as brighter was also higher during the second phase, across most amplitude comparisons. For the third subject, there were measurable but not significant changes, where the first stimuli were perceived as brighter. The effects were consistent within subjects in the three-electrode sequences, where the probability of the reference electrode selected as brighter was correlated to when it was presented in the sequence. CONCLUSIONS: We showed evidence of temporal interactions in non-overlapping sequences of electrodes, where the direction of the effect was subject specific but consistent across a variety of electrode locations and current amplitude levels.

Engineering Artificial Somatosensation Through Cortical Stimulation in Humans.

Sensory feedback is a critical aspect of motor control rehabilitation following paralysis or amputation. Current human studies have demonstrated the ability to deliver some of this sensory information via brain-machine interfaces, although further testing is needed to understand the stimulation parameters effect on sensation. Here, we report a systematic evaluation of somatosensory restoration in humans, using cortical stimulation with subdural mini-electrocorticography (mini-ECoG) grids. Nine epilepsy patients undergoing implantation of cortical electrodes for seizure localization were also implanted with a subdural 64-channel mini-ECoG grid over the hand area of the primary somatosensory cortex (S1). We mapped the somatotopic location and size of receptive fields evoked by stimulation of individual channels of the mini-ECoG grid. We determined the effects on perception by varying stimulus parameters of pulse width, current amplitude, and frequency. Finally, a target localization task was used to demonstrate the use of artificial sensation in a behavioral task. We found a replicable somatotopic representation of the hand on the mini-ECoG grid across most subjects during electrical stimulation. The stimulus-evoked sensations were usually of artificial quality, but in some cases were more natural and of a cutaneous or proprioceptive nature. Increases in pulse width, current strength and frequency generally produced similar quality sensations at the same somatotopic location, but with a perception of increased intensity. The subjects produced near perfect performance when using the evoked sensory information in target acquisition tasks. These findings indicate that electrical stimulation of somatosensory cortex through mini-ECoG grids has considerable potential for restoring useful sensation to patients with paralysis and amputation.

Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation.

Pioneering work with nonhuman primates and recent human studies established intracortical microstimulation (ICMS) in primary somatosensory cortex (S1) as a method of inducing discriminable artificial sensation. However, these artificial sensations do not yet provide the breadth of cutaneous and proprioceptive percepts available through natural stimulation. In a tetraplegic human with two microelectrode arrays implanted in S1, we report replicable elicitations of sensations in both the cutaneous and proprioceptive modalities localized to the contralateral arm, dependent on both amplitude and frequency of stimulation. Furthermore, we found a subset of electrodes that exhibited multimodal properties, and that proprioceptive percepts on these electrodes were associated with higher amplitudes, irrespective of the frequency. These novel results demonstrate the ability to provide naturalistic percepts through ICMS that can more closely mimic the body's natural physiological capabilities. Furthermore, delivering both cutaneous and proprioceptive sensations through artificial somatosensory feedback could improve performance and embodiment in brain-machine interfaces.

Uniform and Non-uniform Perturbations in Brain-Machine Interface Task Elicit Similar Neural Strategies.

The neural mechanisms that take place during learning and adaptation can be directly probed with brain-machine interfaces (BMIs). We developed a BMI controlled paradigm that enabled us to enforce learning by introducing perturbations which changed the relationship between neural activity and the BMI's output. We introduced a uniform perturbation to the system, through a visuomotor rotation (VMR), and a non-uniform perturbation, through a decorrelation task. The controller in the VMR was essentially unchanged, but produced an output rotated at 30° from the neurally specified output. The controller in the decorrelation trials decoupled the activity of neurons that were highly correlated in the BMI task by selectively forcing the preferred directions of these cell pairs to be orthogonal. We report that movement errors were larger in the decorrelation task, and subjects needed more trials to restore performance back to baseline. During learning, we measured decreasing trends in preferred direction changes and cross-correlation coefficients regardless of task type. Conversely, final adaptations in neural tunings were dependent on the type controller used (VMR or decorrelation). These results hint to the similar process the neural population might engage while adapting to new tasks, and how, through a global process, the neural system can arrive to individual solutions.