Title: Sensory prosthetics - clinical and scientific utility of a vestibular implant
Objective: To determine if a vestibular prosthesis could improve function in subjects with severe vestibular damage and could be used it as a scientific tool to investigate central vestibular processing. Background: Damage to the vestibular labyrinth is common and usually permanent. We therefore developed and tested a vestibular implant (VI) that is designed to mimic the information normally provided by the vestibular labyrinth to determine if we can reduce vestibular-mediated deficits and study temporal integration of sensory cues in the brain. Design/Methods: Monkeys had electrodes implanted in the semicircular canals of one ear and then severe bilateral vestibular damage was induced with aminoglycosides. Eye movements, perception, and balance were tested before and after vestibular damage and with the VI activated, which supplied head motion information to the brain via electrical stimulation delivered by the implanted electrodes. Humans also had electrode implantation (done in conjunction with a cochlear implant, CI) and they were tested on a temporal binding psychophysical task Results: Stimulation provided by VI in vestibulopathic monkeys improved their balance, perception of spatial orientation, and eye movement responses. Timing experiments in humans using CI and VI stimuli showed that unlike past experiments that used motion to generate the vestibular signal, CI and VI signals were received by the cerebral cortex with the same latency and were perceived as simultaneous, but this timing perception was highly sensitive to adaption. Conclusions: VI improves oculomotor, postural, and perceptual behavior in vestibulopathic monkeys and could prove to be an effective way to improve these functions in patients with permanent labyrinthine damage. Timing experiments show that when novel stimuli are used, the brain synthesizes them in accordance with their arrival at the cortex, but that experience can rapidly recalibrate this timing relationship, which may be why normal stimuli that are experienced habitually lack this characteristic. more »« less
According to the National Institute of Deafness and other Communication Disorders 2012 report, the number of cochlear implant (CI) users is steadily increasing from 324,000 CI users worldwide. The cochlea, located in the inner ear, is a snail-like structure that exhibits a tonotopic geometry where acoustic waves are filtered spatially according to frequency. Throughout the cochlea, there exist hair cells that transduce sensed acoustic waves into an electrical signal that is carried by the auditory nerve to ultimately reach the auditory cortex of the brain. A cochlear implant bridges the gap if non-functional hair cells are present. Conventional CIs directly inject an electrical current into surrounding tissue via an implanted electrode array and exploit the frequency-to-place mapping of the cochlea. However, the current is dispersed in perilymph, a conductive bodily fluid within the cochlea, causing a spread of excitation. Magnetic fields are more impervious to the effects of the cochlear environment due to the material properties of perilymph and surrounding tissue, demonstrating potential to improve precision. As an alternative to conventional CI electrodes, the development and miniaturization of microcoils intended for micromagnetic stimulation of intracochlear neural elements is described. As a step toward realizing a microcoil array sized for cochlear implantation, human-sized coils were prototyped via aerosol jet printing. The batch reproducible aerosol jet printed microcoils have a diameter of 1800 μm, trace width and trace spacing of 112.5 μm, 12 μm thickness, and inductance values of approximately 15.5 nH. Modelling results indicate that the coils have a combined depolarization–hyperpolarization region that spans 1.5 mm and produce a more restrictive spread of activation when compared with conventional CI.
Letner, Joseph G.; Patel, Paras R.; Hsieh, Jung-Chien; Smith Flores, Israel M.; della Valle, Elena; Walker, Logan A.; Weiland, James D.; Chestek, Cynthia A.; Cai, Dawen
(, Journal of Neural Engineering)
Abstract Objective.Characterizing the relationship between neuron spiking and the signals that electrodes record is vital to defining the neural circuits driving brain function and informing clinical brain-machine interface design. However, high electrode biocompatibility and precisely localizing neurons around the electrodes are critical to defining this relationship.Approach.Here, we demonstrate consistent localization of the recording site tips of subcellular-scale (6.8µm diameter) carbon fiber electrodes and the positions of surrounding neurons. We implanted male rats with carbon fiber electrode arrays for 6 or 12+ weeks targeting layer V motor cortex. After explanting the arrays, we immunostained the implant site and localized putative recording site tips with subcellular-cellular resolution. We then 3D segmented neuron somata within a 50µm radius from implanted tips to measure neuron positions and health and compare to healthy cortex with symmetric stereotaxic coordinates.Main results.Immunostaining of astrocyte, microglia, and neuron markers confirmed that overall tissue health was indicative of high biocompatibility near the tips. While neurons near implanted carbon fibers were stretched, their number and distribution were similar to hypothetical fibers placed in healthy contralateral brain. Such similar neuron distributions suggest that these minimally invasive electrodes demonstrate the potential to sample naturalistic neural populations. This motivated the prediction of spikes produced by nearby neurons using a simple point source model fit using recorded electrophysiology and the mean positions of the nearest neurons observed in histology. Comparing spike amplitudes suggests that the radius at which single units can be distinguished from others is near the fourth closest neuron (30.7 ± 4.6µm, ± S) in layer V motor cortex.Significance.Collectively, these data and simulations provide the first direct evidence that neuron placement in the immediate vicinity of the recording site influences how many spike clusters can be reliably identified by spike sorting.
Lim, J.; Wang, P.T.; Shaw, S.J.; Armacost, M.; Gong, H.; Liu, C.Y.; Heydari, P.; Do, A.H.; Nenadic, Z.
(, Seventh International BCI Meeting, Abstract Book)
Introduction:Current brain-computer interfaces (BCIs) primarily rely on visual feedback. However, visual feedback may not be sufficient for applications such as movement restoration, where somatosensory feedback plays a crucial role. For electrocorticography (ECoG)-based BCIs, somatosensory feedback can be elicited by cortical surface electro-stimulation [1]. However, simultaneous cortical stimulation and recording is challenging due to stimulation artifacts. Depending on the orientation of stimulating electrodes, their distance to the recording site, and the stimulation intensity, these artifacts may overwhelm the neural signals of interest and saturate the recording bioamplifiers, making it impossible to recover the underlying information [2]. To understand how these factors affect artifact propagation, we performed a preliminary characterization of ECoG signals during cortical stimulation.Materials/Methods/ResultsECoG electrodes were implanted in a 39-year old epilepsy patient as shown in Fig. 1. Pairs of adjacent electrodes were stimulated as a part of language cortical mapping. For each stimulating pair, a charge-balanced biphasic square pulse train of current at 50 Hz was delivered for five seconds at 2, 4, 6, 8 and 10 mA. ECoG signals were recorded at 512 Hz. The signals were then high-pass filtered (≥1.5 Hz, zero phase), and the 5-second stimulation epochs were segmented. Within each epoch, artifact-induced peaks were detected for each electrode, except the stimulating pair, where signals were clipped due to amplifier saturation. These peaks were phase-locked across electrodes and were 20 ms apart, thus matching the pulse train frequency. The response was characterized by calculating the median peak within the 5-second epochs. Fig. 1 shows a representative response of the right temporal grid (RTG), with the stimulation channel at RTG electrodes 14 and 15. It also shows a hypothetical amplifier saturation contour of an implantable, bi-directional, ECoG-based BCI prototype [2], assuming the supply voltage of 2.2 V and a gain of 66 dB. Finally, we quantify the worstcase scenario by calculating the largest distance between the saturation contour and the midpoint of each stimulating channel.Discussion:Our results indicate that artifact propagation follows a dipole potential distribution with the extent of the saturation region (the interior of the white contour) proportional to the stimulation amplitude. In general, the artifacts propagated farthest when a 10 mA current was applied with the saturation regions extending from 17 to 32 mm away from the midpoint of the dipole. Consistent with the electric dipole model, this maximum spread happened along the direction of the dipole moment. An exception occurred at stimulation channel RTG11-16, for which an additional saturation contour emerged away from the dipole contour (not shown), extending the saturation region to 41 mm. Also, the worst-case scenario was observed at 6 mA stimulation amplitude. This departure could be a sign of a nonlinear, switch-like behavior, wherein additional conduction pathways could become engaged in response to sufficiently high stimulation.Significance:While ECoG stimulation is routinely performed in the clinical setting, quantitative studies of the resulting signals are lacking. Our preliminary study demonstrates that stimulation artifacts largely obey dipole distributions, suggesting that the dipole model could be used to predict artifact propagation. Further studies are necessary to ascertain whether these results hold across other subjects and combinations of stimulation/recording grids. Once completed, these studies will reveal practical design constraints for future implantable bi-directional ECoG-based BCIs. These include parameters such as the distances between and relative orientations of the stimulating and recording electrodes, the choice of the stimulating electrodes, the optimal placement of the reference electrode, and the maximum stimulation amplitude. These findings would also have important implications for the design of custom, low-power bioamplifiers for implantable bi-directional ECoG-based BCIs.References:[1] Hiremath, S. V., et al. "Human perception of electrical stimulation on the surface of somatosensory cortex." PloS one 12.5 (2017): e0176020.[2] Rouse, A. G., et al. "A chronic generalized bi-directional brain-machine interface." Journal of Neural Engineering 8.3 (2011): 036018
Yusif Rodriguez, Nadira; McKim, Theresa H.; Basu, Debaleena; Ahuja, Aarit; Desrochers, Theresa M.
(, The Journal of Neuroscience)
Monitoring sequential information is an essential component of our daily lives. Many of these sequences are abstract, in that they do not depend on the individual stimuli, but do depend on an ordered set of rules (e.g., chop then stir when cooking). Despite the ubiquity and utility of abstract sequential monitoring, little is known about its neural mechanisms. Human rostrolateral prefrontal cortex (RLPFC) exhibits specific increases in neural activity (i.e., “ramping”) during abstract sequences. Monkey dorsolateral prefrontal cortex (DLPFC) has been shown to represent sequential information in motor (not abstract) sequence tasks, and contains a subregion, area 46, with homologous functional connectivity to human RLPFC. To test the prediction that area 46 may represent abstract sequence information, and do so with parallel dynamics to those found in humans, we conducted functional magnetic resonance imaging (fMRI) in three male monkeys. When monkeys performed no-report abstract sequence viewing, we found that left and right area 46 responded to abstract sequential changes. Interestingly, responses to rule and number changes overlapped in right area 46 and left area 46 exhibited responses to abstract sequence rules with changes in ramping activation, similar to that observed in humans. Together, these results indicate that monkey DLPFC monitors abstract visual sequential information, potentially with a preference for different dynamics in the two hemispheres. More generally, these results show that abstract sequences are represented in functionally homologous regions across monkeys and humans. SIGNIFICANCE STATEMENTDaily, we complete sequences that are “abstract” because they depend on an ordered set of rules (e.g., chop then stir when cooking) rather than the identity of individual items. Little is known about how the brain tracks, or monitors, this abstract sequential information. Based on previous human work showing abstract sequence related dynamics in an analogous area, we tested whether monkey dorsolateral prefrontal cortex (DLPFC), specifically area 46, represents abstract sequential information using awake monkey functional magnetic resonance imaging (fMRI). We found that area 46 responded to abstract sequence changes, with a preference for more general responses on the right and dynamics similar to humans on the left. These results suggest that abstract sequences are represented in functionally homologous regions across monkeys and humans.
Chen, Keying; Forrest, Adam M; Burgos, Guillermo Gonzalez; Kozai, Takashi DY
(, Journal of Neural Engineering)
Abstract Objective.This study aims to reveal longitudinal changes in functional network connectivity within and across different brain structures near chronically implanted microelectrodes. While it is well established that the foreign-body response (FBR) contributes to the gradual decline of the signals recorded from brain implants over time, how the FBR affects the functional stability of neural circuits near implanted brain–computer interfaces (BCIs) remains unknown. This research aims to illuminate how the chronic FBR can alter local neural circuit function and the implications for BCI decoders.Approach.This study utilized single-shank, 16-channel,100µm site-spacing Michigan-style microelectrodes (3 mm length, 703µm2 site area) that span all cortical layers and the hippocampal CA1 region. Sex balanced C57BL6 wildtype mice (11–13 weeks old) received perpendicularly implanted microelectrode in left primary visual cortex. Electrophysiological recordings were performed during both spontaneous activity and visual sensory stimulation. Alterations in neuronal activity near the microelectrode were tested assessing cross-frequency synchronization of local field potential (LFP) and spike entrainment to LFP oscillatory activity throughout 16 weeks after microelectrode implantation.Main results. The study found that cortical layer 4, the input-receiving layer, maintained activity over the implantation time. However, layers 2/3 rapidly experienced severe impairment, leading to a loss of proper intralaminar connectivity in the downstream output layers 5/6. Furthermore, the impairment of interlaminar connectivity near the microelectrode was unidirectional, showing decreased connectivity from Layers 2/3 to Layers 5/6 but not the reverse direction. In the hippocampus, CA1 neurons gradually became unable to properly entrain to the surrounding LFP oscillations.Significance. This study provides a detailed characterization of network connectivity dysfunction over long-term microelectrode implantation periods. This new knowledge could contribute to the development of targeted therapeutic strategies aimed at improving the health of the tissue surrounding brain implants and potentially inform engineering of adaptive decoders as the FBR progresses. Our study’s understanding of the dynamic changes in the functional network over time opens the door to developing interventions for improving the long-term stability and performance of intracortical microelectrodes.
Haburcakova, C., Merfeld, D., Gong, W., Guinand, N., Perez, Fornos A., Thompson, L.A., Guyot, J.P., and Lewis, R.F. Sensory prosthetics - clinical and scientific utility of a vestibular implant. Retrieved from https://par.nsf.gov/biblio/10048831. Neurology 88.16
Haburcakova, C., Merfeld, D., Gong, W., Guinand, N., Perez, Fornos A., Thompson, L.A., Guyot, J.P., & Lewis, R.F. Sensory prosthetics - clinical and scientific utility of a vestibular implant. Neurology, 88 (16). Retrieved from https://par.nsf.gov/biblio/10048831.
Haburcakova, C., Merfeld, D., Gong, W., Guinand, N., Perez, Fornos A., Thompson, L.A., Guyot, J.P., and Lewis, R.F.
"Sensory prosthetics - clinical and scientific utility of a vestibular implant". Neurology 88 (16). Country unknown/Code not available. https://par.nsf.gov/biblio/10048831.
@article{osti_10048831,
place = {Country unknown/Code not available},
title = {Sensory prosthetics - clinical and scientific utility of a vestibular implant},
url = {https://par.nsf.gov/biblio/10048831},
abstractNote = {Objective: To determine if a vestibular prosthesis could improve function in subjects with severe vestibular damage and could be used it as a scientific tool to investigate central vestibular processing. Background: Damage to the vestibular labyrinth is common and usually permanent. We therefore developed and tested a vestibular implant (VI) that is designed to mimic the information normally provided by the vestibular labyrinth to determine if we can reduce vestibular-mediated deficits and study temporal integration of sensory cues in the brain. Design/Methods: Monkeys had electrodes implanted in the semicircular canals of one ear and then severe bilateral vestibular damage was induced with aminoglycosides. Eye movements, perception, and balance were tested before and after vestibular damage and with the VI activated, which supplied head motion information to the brain via electrical stimulation delivered by the implanted electrodes. Humans also had electrode implantation (done in conjunction with a cochlear implant, CI) and they were tested on a temporal binding psychophysical task Results: Stimulation provided by VI in vestibulopathic monkeys improved their balance, perception of spatial orientation, and eye movement responses. Timing experiments in humans using CI and VI stimuli showed that unlike past experiments that used motion to generate the vestibular signal, CI and VI signals were received by the cerebral cortex with the same latency and were perceived as simultaneous, but this timing perception was highly sensitive to adaption. Conclusions: VI improves oculomotor, postural, and perceptual behavior in vestibulopathic monkeys and could prove to be an effective way to improve these functions in patients with permanent labyrinthine damage. Timing experiments show that when novel stimuli are used, the brain synthesizes them in accordance with their arrival at the cortex, but that experience can rapidly recalibrate this timing relationship, which may be why normal stimuli that are experienced habitually lack this characteristic.},
journal = {Neurology},
volume = {88},
number = {16},
author = {Haburcakova, C. and Merfeld, D. and Gong, W. and Guinand, N. and Perez, Fornos A. and Thompson, L.A. and Guyot, J.P. and Lewis, R.F.},
}
Warning: Leaving National Science Foundation Website
You are now leaving the National Science Foundation website to go to a non-government website.
Website:
NSF takes no responsibility for and exercises no control over the views expressed or the accuracy of
the information contained on this site. Also be aware that NSF's privacy policy does not apply to this site.
An official website of the United States government
