Perception of microstimulation frequency in human somatosensory cortex
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Evaluation Summary:
This paper characterizes percepts evoked by micro-stimulating the somatosensory cortex of a human participant. The study provides some new insight into the organization of the human somatosensory cortex and represents an important step in providing more effective somatosensory feedback for brain-machine interface users.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Abstract
Microstimulation in the somatosensory cortex can evoke artificial tactile percepts and can be incorporated into bidirectional brain–computer interfaces (BCIs) to restore function after injury or disease. However, little is known about how stimulation parameters themselves affect perception. Here, we stimulated through microelectrode arrays implanted in the somatosensory cortex of two human participants with cervical spinal cord injury and varied the stimulus amplitude, frequency, and train duration. Increasing the amplitude and train duration increased the perceived intensity on all tested electrodes. Surprisingly, we found that increasing the frequency evoked more intense percepts on some electrodes but evoked less-intense percepts on other electrodes. These different frequency–intensity relationships were divided into three groups, which also evoked distinct percept qualities at different stimulus frequencies. Neighboring electrode sites were more likely to belong to the same group. These results support the idea that stimulation frequency directly controls tactile perception and that these different percepts may be related to the organization of somatosensory cortex, which will facilitate principled development of stimulation strategies for bidirectional BCIs.
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Reviewer #4 (Public Review):
The authors have studied the effects of microstimulation in a single subject with 2 microelectrode arrays in the somatosensory cortex. They aimed to investigate the how altering frequency, current amplitude and train duration affected the elicited percepts. They report three new findings:
Increasing stimulus frequency did not increase the intensity of the percept, in fact there was frequency selectivity of cortical regions and these were somewhat topographically organized on the cortical surface.
The intensity of the subject's responses were similar using suprathreshold (higher) currents but using lowest electrical currents (perithreshold) required higher frequencies for detection similar to other somatosensory brain regions.
Frequency-intensity variation could evoke different types of sensations, with higher …
Reviewer #4 (Public Review):
The authors have studied the effects of microstimulation in a single subject with 2 microelectrode arrays in the somatosensory cortex. They aimed to investigate the how altering frequency, current amplitude and train duration affected the elicited percepts. They report three new findings:
Increasing stimulus frequency did not increase the intensity of the percept, in fact there was frequency selectivity of cortical regions and these were somewhat topographically organized on the cortical surface.
The intensity of the subject's responses were similar using suprathreshold (higher) currents but using lowest electrical currents (perithreshold) required higher frequencies for detection similar to other somatosensory brain regions.
Frequency-intensity variation could evoke different types of sensations, with higher frequencies more likely to evoke tingle or buzz (less natural), and lower frequencies eliciting more pressure, tap, or touch (more natural type sensations).
The major strength of this work is the detailed testing performed over multiple sessions through the same microelectrodes, demonstrating consistent effects. It provides new methods to alter sensations by changing the parameters of stimulation to optimize the type of percept that they are trying to produce.
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Reviewer #3 (Public Review):
Microstimulation of the somatosensory cortex is a very promising approach to restore sensory feedback in disabled people. Hughes and colleagues performed cortical microstimulation experiments in a spinal cord injured subject to characterize the relationship between the stimulation parameters (frequency and amplitude) and the perceived sensation (type and intensity). This type of experiment is very important to better understand the potentials and limits of this approach. The results achieved by the authors are very interesting and can represent a first step towards the development of more effective and personalized approaches to restore sensory feedback. These results need to be confirmed with additional subjects and during closed-loop experiments.
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Reviewer #2 (Public Review):
This study induced tactile percepts through microstimulation via two multi-electrode arrays implanted over a quadriplegic's primary somatosensory hand region. The report focuses on manipulation of the stimulation frequency of microstimulation, though further manipulations were tested and are briefly reported.
For different stimulation sites, the perceived intensity was highest at different stimulation frequencies. This result contradicted the expectation that higher stimulation frequency would be related to higher perceived intensity. This expectation derived from previous work in non-human primates that showed lower detection thresholds for higher-frequency stimulation. The authors show that the same result is obtained in their human patient, suggesting that differences exist between near- and …
Reviewer #2 (Public Review):
This study induced tactile percepts through microstimulation via two multi-electrode arrays implanted over a quadriplegic's primary somatosensory hand region. The report focuses on manipulation of the stimulation frequency of microstimulation, though further manipulations were tested and are briefly reported.
For different stimulation sites, the perceived intensity was highest at different stimulation frequencies. This result contradicted the expectation that higher stimulation frequency would be related to higher perceived intensity. This expectation derived from previous work in non-human primates that showed lower detection thresholds for higher-frequency stimulation. The authors show that the same result is obtained in their human patient, suggesting that differences exist between near- and supra-threshold perceived stimuli and that, accordingly, generalizing from non-human primate work has its traps.
The authors grouped stimulation sites according to optimal stimulation frequency into low, intermediate, and high frequency preferring sites. These three classes were spatially clustered, and related to different patterns of reported perceptual qualities (such as vibration, pressure etc).
The paper's results are important for practical developments of sensory feedback in brain-machine interfaces. Understanding the perceptual result of brain stimulation requires reports by human participants, as underlined by the differences uncovered here between near- and supra-threshold stimulation. They furthermore reveal new aspects of the cortical organisation of primary somatosensory cortex.
The conclusion of clustered patches sensitive to specific frequencies is tentative. As an inherent limitation of intracranial recordings, the total number of stimulation sites is small, and some electrodes did not produce significant results, further reducing the number of analysable sites. Therefore, it is possible that stimulation doesn't truly fall into three distinct clusters (even if such clustering is statistically supported with the current data set), but are actually continuous or divide into a larger number of classes. Notably, this critique does not invalidate the main finding that different patches of cortex show specific frequency preferences.
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Reviewer #1 (Public Review):
This manuscript reports data from unique experiments in which a paralysed person reported sensations evoked by microstimulation of the somatosensory cortex. The main emphasis of this paper is on the effects of increase in stimulation frequency. It was discovered that depending on the electrode used, the peak intensity was felt at different frequencies. Accordingly, the electrodes and stimulation sites were divided into three groups-Low, Intermediate and High frequency preferring. Overall, it was noticed that in most electrodes increasing stimulation frequency beyond about 100 Hz led to less intense sensation. Without knowing the exact somatosensory circuits involved in processing, the connection with recently discovered human vibrotactile psychophysics phenomena and cortical recordings in mice are …
Reviewer #1 (Public Review):
This manuscript reports data from unique experiments in which a paralysed person reported sensations evoked by microstimulation of the somatosensory cortex. The main emphasis of this paper is on the effects of increase in stimulation frequency. It was discovered that depending on the electrode used, the peak intensity was felt at different frequencies. Accordingly, the electrodes and stimulation sites were divided into three groups-Low, Intermediate and High frequency preferring. Overall, it was noticed that in most electrodes increasing stimulation frequency beyond about 100 Hz led to less intense sensation. Without knowing the exact somatosensory circuits involved in processing, the connection with recently discovered human vibrotactile psychophysics phenomena and cortical recordings in mice are speculative, but are in close agreement with the current observation and thus the manuscript would benefit from expanding discussion on this. I personally don't think there is any contradiction with non-human primate studies, as the authors state, rather it should be viewed as a significant extension to those studies and warrants viewing them in a new light.
A very interesting observation is that three types of frequency-intensity effects are associated with different perceptual qualities. However, types of seemingly distinct sensations might be attributed to semantics describing sensation of periodic stimulation at different intensities. Subjective reports of one subject are very valuable to set future directions for this kind of investigation, but may not be enough to generalise those findings just yet.
The location of electrodes belonging to three different frequency-intensity effect groups appeared to be not at random, but whether it reflects cortical organisation or some other factors like systematic variation in electrode depth might have influenced the result, needs to be confirmed. Only a small number of electrodes was tested - 8 in the Medial Array and 11 in the Lateral Array.
Three frequency-intensity effect group electrodes also differed in median intensity reported across all frequencies, which cautions that the reported perceptual quality differences at least partly might be attributed to the overall level of intensity sensation. It has to be noted that the overall frequency-intensity response profile did not change by changing the stimulation current, however some shifts seems to be present. Alternatively, such frequency-intensity effect profiles represent circuits tuned to detection of specific features of stimuli. This possibility is indeed very intriguing.
As those experiments performed on a human subject with implanted electrodes are absolutely unique, the data are exceptionally interesting regardless of limitations generalising those findings. Unlike animal experiments humans can describe sensations evoked by cortical microstimulation so there is no substitution for these experiments and every piece of evidence is highly valuable. These results give ground for new hypotheses to better understand how the somatosensory system works and generate ideas for designing future human psychophysics and animal model experiments. From a practical point of view, it is exceptionally valuable for informing the design of stimulation protocols for bidirectional brain-computer interfaces (BCIs).
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Evaluation Summary:
This paper characterizes percepts evoked by micro-stimulating the somatosensory cortex of a human participant. The study provides some new insight into the organization of the human somatosensory cortex and represents an important step in providing more effective somatosensory feedback for brain-machine interface users.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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