Americo A. Migliaccio

A Multichannel Semicircular Canal Neural Prosthesis Using Electrical Stimulation to Restore 3-D Vestibular Sensation

Bilateral loss of vestibular sensation can be disabling. Those afflicted suffer illusory visual field movement during head movements, chronic disequilibrium and postural instability due to failure of vestibulo-ocular and vestibulo-spinal reflexes. A neural prosthesis that emulates the normal transduction of head rotation by semicircular canals could significantly improve quality of life for these patients. Like the three semicircular canals in a normal ear, such a device should at least transduce three orthogonal (or linearly separable) components of head rotation into activity on corresponding ampullary branches of the vestibular nerve. We describe the design, circuit performance and in vivo application of a head-mounted, semi-implantable multichannel vestibular prosthesis that encodes head movement in three dimensions as pulse-frequency-modulated electrical stimulation of three or more ampullary nerves. In chinchillas treated with intratympanic gentamicin to ablate vestibular sensation bilaterally, prosthetic stimuli elicited a partly compensatory angular vestibulo-ocular reflex in multiple planes. Minimizing misalignment between the axis of eye and head rotation, apparently caused by current spread beyond each electrodes targeted nerve branch, emerged as a key challenge. Increasing stimulation selectivity via improvements in electrode design, surgical technique and stimulus protocol will likely be required to restore AVOR function over the full range of normal behavior

Semicircular canal function before and after surgery for superior canal dehiscence.

Objective: To characterize semicircular canal function before and after surgery for superior semicircular canal dehiscence (SCD) syndrome. Study Design: Prospective unblinded study of physiologic effect of intervention. Setting: Tertiary referral center. Patients: Patients with SCD syndrome documented by history, sound- or pressure-evoked eye movements, vestibular-evoked myogenic potential testing, and high-resolution multiplanar computed tomographic scans. Intervention: Nineteen subjects with SCD had quantitative measurements of their angular vestibulo-ocular reflexes (AVOR) in response to rapid rotary head thrusts measured by magnetic search coil technique before and after middle fossa approach and repair of the dehiscence. In 18 subjects, the dehiscence was plugged; and in 1, it was resurfaced. Main Outcome Measures: The AVOR gains (eye velocity/head velocity) for excitation of each of the semicircular canals. Results: Vertigo resulting from pressure or loud sounds resolved in each case. Before surgery, mean AVOR gains were normal for the ipsilateral horizontal (0.94 ± 0.07) and posterior (0.84 ± 0.09) canals. For the superior canal to be operated on, AVOR gain was 0.75 ± 0.13; but this was not significantly lower than the gain for the contralateral superior canal (0.82 ± 0.11, p = 0.08). Mean AVOR gain decreased by 44% for the operated superior canals (to 0.42 ± 0.11, p < 0.0001). There was a 13% decrease in gain for the ipsilateral posterior canal (p = 0.02), perhaps because plugging affected the common crus in some cases. There was a 10% decrease in gain for excitation of the contralateral posterior canal (p < 0.0001), which likely reflects the loss of the inhibitory contribution of the plugged superior canal during head thrusts exciting the contralateral posterior canal. Mean AVOR gain did not change for any of the other canals, but two subjects did develop hypofunction of all three ipsilateral canals postoperatively. Conclusion: Middle fossa craniotomy and repair of SCD reduce the function of the operated superior canal but typically preserve the function of the other ipsilateral semicircular canals.

Mechanism of Dynamic Visual Acuity Recovery With Vestibular Rehabilitation

OBJECTIVE To determine why dynamic visual acuity (DVA) improves after vestibular rehabilitation in people with vestibular hypofunction. DESIGN Combined descriptive and intervention study. SETTING Outpatient department in an academic medical institution. PARTICIPANTS Five patients (age, 42-66 y) and 4 age-matched controls (age, 39-67 y) were studied. Patients had vestibular hypofunction (mean duration, 177+/-188 d) identified by clinical (positive head thrust test, abnormal DVA), physiologic (reduced angular vestibulo-ocular reflex [aVOR] gain during passive head thrust testing), and imaging examinations (absence of tumor in the internal auditory canals or cerebellopontine angle). INTERVENTION Vestibular rehabilitation focused on gaze and gait stabilization (mean, 5.0+/-1.4 visits; mean, 66+/-24 d). The control group did not receive any intervention. MAIN OUTCOME MEASURES aVOR gain (eye velocity/head velocity) during DVA testing (active head rotation) and horizontal head thrust testing (passive head rotation) to control for spontaneous recovery. RESULTS For all patients, DVA improved (mean, 51%+/-25%; range, 21%-81%). aVOR gain during the active DVA test increased in each of the patients (mean range, 0.7+/-0.2 to 0.9+/-0.2 [35%]). aVOR gain during passive head thrust did not improve in 3 patients and improved only partially in the other 2. For control subjects, aVOR gain during DVA was near 1. CONCLUSIONS Our data suggest that vestibular rehabilitation increases aVOR gain during active head rotation independent of peripheral aVOR gain recovery.

Search-coil head-thrust and caloric tests in Ménière's disease

Conclusions. Our findings suggest that canal function is substantially preserved in subjects with active vertigo attacks as a result of Ménières disease (MD). In these subjects, the head-thrust test (HTT) may not be as sensitive to canal dysfunction as traditional caloric testing. MD may differentially affect the low-frequency sensitivity of the canals. Objective. Caloric tests have traditionally been used to characterize semicircular canal function in vestibular disorders, including MD. The quantitative HTT provides an objective measurement of semicircular canal function in the frequency and velocity ranges of normal head movements. The aim of this study was to compare the findings of caloric and HTTs in subjects with unilateral MD. Material and methods. The study population consisted of 38 candidates for gentamicin treatment due to a high frequency of vertiginous attacks (25 males, 13 females; mean age 52.9 years; range 30–70 years). The duration of symptoms was 1–30 years (mean 5.3 years). Horizontal canal function was characterized with bithermal aqueous caloric tests and recordings of the angular vestibulo-ocular reflexes (aVORs) using the scleral search-coil technique during HTTs. The main outcomes were unilateral weakness (UW) on caloric testing and aVOR gain asymmetry (GA) during HTTs. A caloric response asymmetry of >20% was considered to be indicative of pathologic UW. A difference in GA during HTTs of >5.8% was considered significant. Results. Twenty subjects (52.6%) showed abnormal results on one or both tests. Pathologic UW was present in 16 subjects (42.1%). During HTTs, 11 subjects (28.9%) showed pathologic GA. Seven subjects (18.4%) showed abnormal results on both tests. A significant correlation was found between UW and GA. However, pathologic GA during HTTs in subjects with unilateral MD was less frequent and the values smaller than those published for vestibular neuritis patients. Two subjects with unilateral MD had 100% UW, but none had >30% asymmetry on HTTs.

Dynamic Visual Acuity during Passive Head Thrusts in Canal Planes

We sought to determine whether the dynamic visual acuity (DVA) test, which has been used to measure the function of the two horizontal semicircular canals (SCCs), could be adapted to measure the individual function of all six SCCs using transient, rapid, unpredictable head rotation stimuli (head thrusts) in the direction of maximum sensitivity of each SCC. We examined head-thrust DVA (htDVA) performance in 19 healthy control subjects, five patients before and six patients after plugging of one superior SCC for treatment of superior canal dehiscence, and two subjects with unilateral vestibular deafferentation (UVD) by vestibular neurectomy. We compared htDVA results for each SCC to vestibulo-ocular reflex gains measured using 3-D scleral coil recordings during a passive head-thrust-test paradigm. Individuals with normal vestibular function had similar htDVA scores for each of the six directions (canals) tested (mean 0.058 ± 0.050 LogMAR). Individuals tested after surgical plugging of one superior SCC were similar to normal for all SCCs except the plugged SCC, which had significantly worse htDVA scores (mean 0.270 ± 0.08 LogMAR). Individuals with UVD had significantly worse htDVA scores for head rotations maximally exciting any of the ipsilesional SCC (mean 0.317 ± 0.129 LogMAR) and scores similar to normal subjects for contralesional rotations (0.063 ± 0.051 LogMAR). These findings suggest that the htDVA test, which does not require scleral coil placement, magnetic field coils, or expensive oculography equipment, can provide a useful quantitative measure of individual SCC function.

Vestibulo-Ocular Reflex Responses to a Multichannel Vestibular Prosthesis Incorporating a 3D Coordinate Transformation for Correction of Misalignment

There is no effective treatment available for individuals unable to compensate for bilateral profound loss of vestibular sensation, which causes chronic disequilibrium and blurs vision by disrupting vestibulo-ocular reflexes that normally stabilize the eyes during head movement. Previous work suggests that a multichannel vestibular prosthesis can emulate normal semicircular canals by electrically stimulating vestibular nerve branches to encode head movements detected by mutually orthogonal gyroscopes affixed to the skull. Until now, that approach has been limited by current spread resulting in distortion of the vestibular nerve activation pattern and consequent inability to accurately encode head movements throughout the full 3-dimensional (3D) range normally transduced by the labyrinths. We report that the electrically evoked 3D angular vestibulo-ocular reflex exhibits vector superposition and linearity to a sufficient degree that a multichannel vestibular prosthesis incorporating a precompensatory 3D coordinate transformation to correct misalignment can accurately emulate semicircular canals for head rotations throughout the range of 3D axes normally transduced by a healthy labyrinth.

Evaluation of quantitative head impulse testing using search coils versus video-oculography in older individuals

Objective To evaluate the validity of 2D video-oculography (VOG) compared with scleral search coils for horizontal AVOR gain estimation in older individuals. Study Design Cross-sectional validation study. Setting Tertiary care academic medical center. Patients Six individuals age 70 and older. Interventions Simultaneous eye movement recording with scleral search coil (over right eye) and EyeSeeCam VOG camera (over left eye) during horizontal head impulses. Main Outcome Measures Best estimate search coil and VOG horizontal AVOR gain, presence of compensatory saccades using both eye movement recording techniques. Results We observed a significant correlation between search coil and VOG best estimate horizontal AVOR gain (r = 0.86, p = 0.0002). We evaluated individual head impulses and found that the shapes of the head movement and eye movement traces from the coil and VOG systems were similar. Specific features of eye movements seen in older individuals, including overt and covert corrective saccades and anticompensatory eye movements, were captured by both the search coil and VOG systems. Conclusion These data suggest that VOG is a reasonable proxy for search coil eye movement recording in older subjects to estimate VOR gain and the approximate timing of corrective eye movements. VOG offers advantages over the conventional search coil method; it is portable and easy to use, allowing for quantitative VOR estimation in diverse settings such as a routine office-based practice, at the bedside, and potentially in larger scale population analyses.

The Vestibulo-ocular Reflex Response to Head Impulses Rarely Decreases after Cochlear Implantation

Objective: Measure vestibular function using the head impulse test and assess the change in function due to unilateral cochlear implantation. Background: Cochlear implantation entails risks to vestibular function in the implanted ear. However, the nature and extent of this risk is not known. The head impulse test uses physiologically relevant stimuli that allow detection of subtle changes in vestibular function of individual semicircular canals. Subjects: Sixteen adults (age, 28-65 years) were recruited for prospective study from the Listening Center at Johns Hopkins. Eleven of these subjects were tested 4 to 6 weeks after cochlear implantation. Methods: Three-dimensional eye movement recordings were made using the scleral search coil technique. Stimuli were rapid, passive, transient, head-on-body rotations (acceleration ∼3000°/s2) in the direction excitatory for each of the six semicircular canals. Results: Of the 16 subjects measured preoperatively, 6 (36%) had low (<0.74) VOR gains in one or both of the horizontal canals and 8 (50%) had low (<0.64) vestibulo-ocular reflex (VOR) gains in one or more of the vertical canals. These preoperative gain deficits were bilateral in six subjects. The VOR gain did not significantly change after implantation in 10 out of the 11 subjects tested postoperatively. The remaining subject suffered a partial loss of function in the implanted ear and was the only subject who experienced transient vertigo and oscillopsia after implantation. Conclusions: Preoperative vestibular deficits were common among this group of candidates for cochlear implantation; however, significant loss of vestibular function due to cochlear implantation was uncommon.

Electrical Stimulation to Restore Vestibular Function Development of a 3-D Vestibular Prosthesis

Patients who fail to compensate for bilateral loss of vestibular sensory function are disabled by disequilibrium and illusory movement of the visual field during head movement. An implantable prosthesis that restores vestibular sensation could significantly improve quality of life for these patients. To be effective, such a device should encode head rotation in all 3 dimensions. We describe the 3-dimensional angular vestibulo-ocular reflex of normal chinchillas and vestibular-deficient chinchillas undergoing functional electrical stimulation of the vestibular nerve. We also describe the design and fabrication of a head-mounted, 8 electrode vestibular prosthesis that encodes head movement in 3 dimensions

Vestibulo-ocular reflex pathways in internuclear ophthalmoplegia

We measured the vestibulo‐ocular reflex (VOR) during head impulses in a patient with right‐sided internuclear ophthalmoplegia. Head impulses are rapid, passive, high‐acceleration, low‐amplitude head rotations in the direction of a particular semicircular canal (SCC). Adduction of the right eye was abnormally slow during right lateral SCC head impulses. The VOR during left posterior SCC impulses was severely deficient in both eyes, but the VOR during left anterior SCC impulses was only slightly deficient. We suggest that the vertical vestibulo‐ocular pathways in humans are connected in SCC‐plane coordinates, not the traditional roll and pitch coordinates, and that anterior SCC signals do not travel exclusively in the medial longitudinal fasciculus. Ann Neurol 1999;45:529–533