To investigate the neural mechanisms that humans use to process the ambiguous force measured by the otolith organs, we measured vestibuloocular reflexes (VORs) and perceptions of tilt and translation. One primary goal was to determine if the same, or different, mechanisms contribute to vestibular perception and action. We used motion paradigms that provided identical sinusoidal inter-aural otolith cues across a broad frequency range. We accomplished this by sinusoidally tilting (20 degrees, 0.005-0.7 Hz) subjects in roll about an earth-horizontal, head-centered, rotation axis ("Tilt") or sinusoidally accelerating (3.3 m/s2, 0.005-0.7 Hz) subjects along their inter-aural axis ("Translation"). While identical inter-aural otolith cues were provided by these motion paradigms, the canal cues were substantially different because roll rotations were present during Tilt but not during Translation. We found that perception was dependent on canal cues because the reported perceptions of both roll tilt and inter-aural translation were substantially different during Translation and Tilt. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs at frequencies >0.2 Hz during both Translation and Tilt. These responses were dependent on otolith cues and match simple filtering predictions that translational VORs include contributions via simple high-pass filtering of otolith cues. More generally, these findings demonstrate that internal models govern human vestibular "perception" across a broad range of frequencies and that simple high-pass filters contribute to human horizontal translational VORs ("action") at frequencies above approximately 0.2 Hz.
To compare and contrast the neural mechanisms that contribute to vestibular perception and action, we measured vestibuloocular reflexes (VOR) and perceptions of tilt and translation. We took advantage of the well-known ambiguity that the otolith organs respond to both linear acceleration and tilt with respect to gravity and investigated the mechanisms by which this ambiguity is resolved. A new motion paradigm that combined roll tilt with inter-aural translation ("Tilt&Translation") was used; subjects were sinusoidally (0.8 Hz) roll tilted but with their ears above or below the rotation axis. This paradigm provided sinusoidal roll canal cues that were the same across trials while providing otolith cues that varied linearly with ear position relative to the earth-horizontal rotation axis. We found that perceived tilt and translation depended on canal cues, with substantial roll tilt and inter-aural translation perceptions reported even when the otolith organs measured no inter-aural force. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs that varied linearly with radius; a minimal response was measured when the otolith organs transduced little or no inter-aural force. Hence, the horizontal translational VOR was dependent on otolith cues but independent of canal cues. These findings match predictions that translational VORs are elicited by simple filtering of otolith signals. We conclude that internal models govern human perception of tilt and translation at 0.8 Hz and that high-pass filtering governs the human translational VOR at this same frequency.
Stochastic resonance (SR) is a phenomenon whereby the response of a non-linear system to a weak periodic input signal is optimized by the presence of a particular non-zero level of noise. Stochastic resonance using imperceptible stochastic vestibular electrical stimulation, when applied to normal young and elderly subjects, has been shown to significantly improve ocular stabilization reflexes in response to whole-body tilt; improved balance performance during postural disturbances and optimize covariance between the weak input periodic signals introduced via venous blood pressure receptors and the heart rate responses. In our study, 15 subjects stood on a compliant surface with their eyes closed. They were given low-amplitude binaural bipolar stochastic electrical stimulation of the vestibular organs in two frequency ranges of 1-2 and 0-30 Hz over the amplitude range of 0 to ±700 μA. Subjects were instructed to maintain an upright stance during 43-s trials, which consisted of baseline (zero amplitude) and stimulation (non-zero amplitude) periods. Measures of stability of the head and trunk using inertial motion unit sensors attached to these segments and the whole body using a force plate were measured and quantified in the mediolateral plane. Using a multivariate optimization criterion, our results show that the low levels of vestibular stimulation given to the vestibular organs improved balance performance in normal healthy subjects in the range of 5-26% consistent with the stochastic resonance phenomenon. In our study, 8 of 15 and 10 of 15 subjects were responsive for the 1-2- and 0-30-Hz stimulus signals, respectively. The improvement in balance performance did not differ significantly between the stimulations in the two frequency ranges. The amplitude of optimal stimulus for improving balance performance was predominantly in the range of ±100 to ±400 μA. A device based on SR stimulation of the vestibular system might be useful as either a training modality to enhance adaptability or skill acquisition, or as a miniature patch-type stimulator that may be worn by people with disabilities due to aging or disease to improve posture and locomotion function.
Objective:Patients with peripheral vestibular dysfunction because of gravitational receptor asymmetries display signs of cognitive dysfunction and are assumed to have neurobehavioral sequelae. This was tested with pre- and postoperatively quantitative measurements in three cohort groups with superior semicircular canal dehiscence syndrome (SSCDS) symptoms with: 1) superior canal dehiscence (SCD) repaired via a middle cranial fossa craniotomy and canal plugging only; 2) otic capsule defects not visualized with imaging (no-iOCD) repaired with round window reinforcement (RWR) only; or 3) both SCD plugging and subsequent development of no-iOCD followed by RWR.Study Design:Prospective patient series.Setting:Tertiary referral center.Patients:There were 13 adult and 4 pediatric patients with SSCDS who had completion of neuropsychology test batteries pre- and every 3 months postoperatively. Eight patients had no-iOCD and RWR exclusively, 5 had SCD and plugging exclusively, and 4 had both SCD plugging and then development of no-iOCD with RWR. These cohorts included SSCDS with 2 different dehiscence locations.Interventions:Completion of a neuropsychology test battery preoperatively and at 3, 6, 9, and 12 months postoperatively that included: Beck Depression Inventory-II (BDI); Wide Range Intelligence Test (WRIT FSIQ) including average verbal (crystallized intelligence) and visual (fluid intelligence); Wide Range Assessment of Memory and Learning (WRAML), including the four domains of verbal memory, visual memory, attention/concentration, and working memory; and Delis–Kaplan Executive Function System (D-KEFS). The Dizziness Handicap Inventory (DHI) and the Headache Impact Test (HIT-6) were also completed to assess the impact of their disease on activities pre- and postoperatively.Main Outcome Measures:Quantitative and statistical analysis of their cognitive and neurobehavioral function.Results:The pattern of differences between the SCD group and the no-iOCD group from WRAML verbal, visual, and attention test performance indicate different postoperative clinical trajectories. For the WRAML, there was a statistically significant improvement for visual memory and verbal memory for the no-iOCD only and both (SCD and subsequent no-iOCD) groups, but no mean improvement for the SCD only group. By contrast, the no-iOCD group had significantly lower scores on the WRAML attention test preoperatively, but they recovered postoperatively to match the other groups. The preoperative findings and postoperative outcomes did not differ significantly among patient groups on the WRAML working memory test, D-KEFS motor scores, D-KEFS number and letter scores, or Wide Range Intelligence Test scores. There was a significant decrease in the BDI for all groups. The IQ scores were unchanged. There was a statistically significant improvement in the DHI and HIT-6 scores postoperatively in all groups.Conclusions:There was a marked overall improvement in cognitive and neurobehavioral function postoperatively. Variability may result from duration of unde...
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