scholarly journals Integration of vestibular and hindlimb inputs by vestibular nucleus neurons: Multisensory influences on postural control

2019 ◽  
Author(s):  
Derek M. Miller ◽  
Carey D. Balaban ◽  
Andrew A. McCall

1.AbstractWe recently demonstrated in both decerebrate and conscious cat preparations that hindlimb somatosensory inputs converge with vestibular afferent input onto neurons in multiple CNS locations that participate in balance control. While it is known that head position and limb state modulate postural reflexes, presumably through both vestibulospinal and reticulospinal pathways, the combined influence of the two inputs on the activity of neurons in these brainstem regions is unknown. In the present study, we evaluated the responses of vestibular nucleus (VN) neurons to vestibular and hindlimb stimuli delivered separately and together in conscious cats. We hypothesized that VN neuronal firing during activation of vestibular and limb proprioceptive inputs would be well-fit by an additive model. Extracellular single-unit recordings were obtained from neurons in the caudal aspects of the VN. Sinusoidal whole-body rotation in the roll plane was used as the search stimulus. Units responding to the search stimulus were tested for their responses to 10° ramp-and-hold roll body rotation, 10° extension hindlimb movement, and both movements delivered simultaneously. Composite response histograms were fit by a model of low and high pass filtered limb and body position signals using least squares nonlinear regression. We found that VN neuronal activity during combined vestibular and hindlimb proprioceptive stimulation in the conscious cat is well-fit by a simple additive model for signals with similar temporal dynamics. The mean R2 value for goodness of fit across all units was 0.74 ± 0.17. It is likely that VN neurons that exhibit these integrative properties participate in adjusting vestibulospinal outflow in response to limb state.New and NoteworthyVestibular nucleus neurons receive convergent information from hindlimb somatosensory inputs and vestibular inputs. In this study, extracellular single unit recordings of vestibular nucleus neurons during conditions of passively applied limb movement, passive whole-body rotations, and combined stimulation, were well fit by an additive model. The integration of hindlimb somatosensory inputs with vestibular inputs at the first stage of vestibular processing suggests vestibular nucleus neurons account for limb position in determining vestibulospinal responses to postural perturbations.

2021 ◽  
Vol 125 (4) ◽  
pp. 1095-1110
Author(s):  
Andrew A. McCall ◽  
Derek M. Miller ◽  
Carey D. Balaban

Vestibular nucleus neurons receive convergent information from hindlimb somatosensory inputs and vestibular inputs. In this study, extracellular single-unit recordings of vestibular nucleus neurons during conditions of passively applied limb movement, passive whole body rotations, and combined stimulation were well fit by an additive model. The integration of hindlimb somatosensory inputs with vestibular inputs at the first stage of vestibular processing suggests that vestibular nucleus neurons account for limb position in determining vestibulospinal responses to postural perturbations.


2017 ◽  
Author(s):  
Masanori Shimono ◽  
Naomichi Hatano

AbstractGlobal dynamics in the brain can be captured using fMRI, MEG, or electrocorticography (ECoG), but models are often restricted by anatomical constraints. Complementary single-/multi-unit recordings have described local fast temporal dynamics. However, because of anatomical constraints, global fast temporal dynamics remain incompletely understood. Therefore, we compared temporal aspects of cross-area propagations of single-unit recordings and ECoG, and investigated their anatomical bases. First, we demonstrated how both evoked and spontaneous ECoGs can accurately predict latencies of single-unit recordings. Next, we estimated the propagation velocity (1.0–1.5 m/s) from brain-wide data and found that it was fairly stable among different conscious levels. We also found that the anatomical topology strongly predicted the latencies. Finally, Communicability, a novel graph-theoretic measure, could systematically capture the balance between shorter or longer pathways. These results demonstrate that macro-connectomic perspective is essential for evaluating detailed temporal dynamics in the brain.Author SummaryThis study produced four main findings: First, we demonstrated that ECoG signals could predict the timing of evoked electrical spikes of neurons elicited by visual stimuli. Second, we showed that spontaneous ECoG recorded under a blindfold condition (without any stimuli) could also predict the timing of visually evoked neuronal spikes. We also clarified that performance predictions from blindfold data are essentially supported by the constraints of structural paths. Third, we quantified the propagation velocity (conductance velocity) as 1.0–1.5 m/s, and found that the velocity was stable among different conscious levels. Fourth, Communicability successfully characterized the relative contributions of shorter and longer paths. This study represents an important contribution to the theoretical understanding of the brain in terms of connectomics, dynamical propagations, and multi-scale architectures.


1999 ◽  
Vol 82 (1) ◽  
pp. 436-449 ◽  
Author(s):  
Greg T. Gdowski ◽  
Robert A. McCrea

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20°/s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non–eye-movement ( n = 52) and eye-movement–related ( n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 ± 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement–related units tended to have rotational responses that were correlated with head velocity. On the other hand, non–eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.


2016 ◽  
Vol 116 (4) ◽  
pp. 1785-1794 ◽  
Author(s):  
Andrew A. McCall ◽  
Derek M. Miller ◽  
William M. DeMayo ◽  
George H. Bourdages ◽  
Bill J. Yates

The limbs constitute the sole interface with the ground during most waking activities in mammalian species; it is therefore expected that somatosensory inputs from the limbs provide important information to the central nervous system for balance control. In the decerebrate cat model, the activity of a subset of neurons in the vestibular nuclei (VN) has been previously shown to be modulated by hindlimb movement. However, decerebration can profoundly alter the effects of sensory inputs on the activity of brain stem neurons, resulting in epiphenomenal responses. Thus, before this study, it was unclear whether and how somatosensory inputs from the limb affected the activity of VN neurons in conscious animals. We recorded brain stem neuronal activity in the conscious cat and characterized the responses of VN neurons to flexion and extension hindlimb movements and to whole body vertical tilts (vestibular stimulation). Among 96 VN neurons whose activity was modulated by vestibular stimulation, the firing rate of 65 neurons (67.7%) was also affected by passive hindlimb movement. VN neurons in conscious cats most commonly encoded hindlimb movement irrespective of the direction of movement ( n = 33, 50.8%), in that they responded to all flexion and extension movements of the limb. Other VN neurons overtly encoded information about the direction of hindlimb movement ( n = 27, 41.5%), and the remainder had more complex responses. These data confirm that hindlimb somatosensory and vestibular inputs converge onto VN neurons of the conscious cat, suggesting that VN neurons integrate somatosensory inputs from the limbs in computations that affect motor outflow to maintain balance.


2004 ◽  
Vol 96 (3) ◽  
pp. 923-930 ◽  
Author(s):  
L. A. Cotter ◽  
H. E. Arendt ◽  
S. P. Cass ◽  
B. J. Jian ◽  
D. F. Mays ◽  
...  

Previous studies in humans showed that genioglossal muscle activity is higher when individuals are supine than when they are upright, and prior experiments in anesthetized or decerebrate animals suggested that vestibular inputs might participate in triggering these alterations in muscle firing. The present study determined the effects of whole body tilts in the pitch (nose-up) plane on genioglossal activity in a conscious feline model and compared these responses with those generated by roll (ear-down) tilts. We also ascertained the effects of a bilateral vestibular neurectomy on the alterations in genioglossal activity elicited by changes in body position. Both pitch and roll body tilts produced modifications in muscle firing that were dependent on the amplitude of the rotation; however, the relative effects of ear-down and nose-up tilts on genioglossal activity were variable from animal to animal. The response variability observed might reflect the fact that genioglossus has a complex organization and participates in a variety of tongue movements; in each animal, electromyographic recordings presumably sampled the firing of different proportions of fibers in the various compartments and subcompartments of the muscle. Furthermore, removal of labyrinthine inputs resulted in alterations in genioglossal responses to postural changes that persisted until recordings were discontinued ∼1 mo later, demonstrating that the vestibular system participates in regulating the muscle's activity. Peripheral vestibular lesions were subsequently demonstrated to be complete through the postmortem inspection of temporal bone sections or by observing that vestibular nucleus neurons did not respond to rotations in vertical planes.


2002 ◽  
Vol 13 (04) ◽  
pp. 188-204 ◽  
Author(s):  
Shigeyuki Kuwada ◽  
Julia S. Anderson ◽  
Ranjan Batra ◽  
Douglas C. Fitzpatrick ◽  
Natacha Teissier ◽  
...  

The scalp-recorded amplitude-modulation following response (AMFR)” is gaining recognition as an objective audiometric tool, but little is known about the neural sources that underlie this potential. We hypothesized, based on our human studies and single-unit recordings in animals, that the scalp-recorded AMFR reflects the interaction of multiple sources. We tested this hypothesis using an animal model, the unanesthetized rabbit. We compared AMFRs recorded from the surface of the brain at different locations and before and after the administration of agents likely to enhance or suppress neural generators. We also recorded AMFRs locally at several stations along the auditory neuraxis. We conclude that the surface-recorded AMFR is indeed a composite response from multiple brain generators. Although the response at any modulation frequency can reflect the activity of more than one generator, the AMFRs to low and high modulation frequencies appear to reflect a strong contribution from cortical and subcortical sources, respectively.


Risks ◽  
2021 ◽  
Vol 9 (3) ◽  
pp. 53
Author(s):  
Yves Staudt ◽  
Joël Wagner

For calculating non-life insurance premiums, actuaries traditionally rely on separate severity and frequency models using covariates to explain the claims loss exposure. In this paper, we focus on the claim severity. First, we build two reference models, a generalized linear model and a generalized additive model, relying on a log-normal distribution of the severity and including the most significant factors. Thereby, we relate the continuous variables to the response in a nonlinear way. In the second step, we tune two random forest models, one for the claim severity and one for the log-transformed claim severity, where the latter requires a transformation of the predicted results. We compare the prediction performance of the different models using the relative error, the root mean squared error and the goodness-of-lift statistics in combination with goodness-of-fit statistics. In our application, we rely on a dataset of a Swiss collision insurance portfolio covering the loss exposure of the period from 2011 to 2015, and including observations from 81 309 settled claims with a total amount of CHF 184 mio. In the analysis, we use the data from 2011 to 2014 for training and from 2015 for testing. Our results indicate that the use of a log-normal transformation of the severity is not leading to performance gains with random forests. However, random forests with a log-normal transformation are the favorite choice for explaining right-skewed claims. Finally, when considering all indicators, we conclude that the generalized additive model has the best overall performance.


2021 ◽  
pp. 464-469
Author(s):  
Dominik Péus ◽  
Dominik Straumann ◽  
Alexander Huber ◽  
Christopher J. Bockisch ◽  
Vincent Wettstein

Downbeat nystagmus (DBN) observed in head-hanging positions, may be of central or peripheral origin. Central DBN in head-hanging positions is mostly due to a disorder of the vestibulo-cerebellum, whereas peripheral DBN is usually attributed to canalolithiasis of an anterior semicircular canal. Here, we describe an atypical case of a patient who, after head trauma, experienced severe and stereotypic vertigo attacks after being placed in various head-hanging positions. Vertigo lasted 10–15 s and was always associated with a robust DBN. The provocation of transient vertigo and DBN, which both showed no decrease upon repetition of maneuvers, depended on the yaw orientation relative to the trunk and the angle of backward pitch. On a motorized, multi-axis turntable, we identified the two-dimensional Helmholtz coordinates of head positions at which vertigo and DBN occurred (<i>y</i>-axis: horizontal, space-fixed; <i>z</i>-axis: vertical, and head-fixed; <i>x</i>-axis: torsional, head-fixed, and unchanged). This two-dimensional area of DBN-associated head positions did not change when whole-body rotations took different paths (e.g., by forwarding pitch) or were executed with different velocities. Moreover, the intensity of DBN was also independent of whole-body rotation paths and velocities. So far, therapeutic approaches with repeated liberation maneuvers and cranial vibrations were not successful. We speculate that vertigo and DBN in this patient are due to macular damage, possibly an unstable otolithic membrane that, in specific orientations relative to gravity, slips into a position causing paroxysmal stimulation or inhibition of macular hair cells.


2021 ◽  
Vol 11 (6) ◽  
pp. 761
Author(s):  
Gert Dehnen ◽  
Marcel S. Kehl ◽  
Alana Darcher ◽  
Tamara T. Müller ◽  
Jakob H. Macke ◽  
...  

Single-unit recordings in the brain of behaving human subjects provide a unique opportunity to advance our understanding of neural mechanisms of cognition. These recordings are exclusively performed in medical centers during diagnostic or therapeutic procedures. The presence of medical instruments along with other aspects of the hospital environment limit the control of electrical noise compared to animal laboratory environments. Here, we highlight the problem of an increased occurrence of simultaneous spike events on different recording channels in human single-unit recordings. Most of these simultaneous events were detected in clusters previously labeled as artifacts and showed similar waveforms. These events may result from common external noise sources or from different micro-electrodes recording activity from the same neuron. To address the problem of duplicate recorded events, we introduce an open-source algorithm to identify these artificial spike events based on their synchronicity and waveform similarity. Applying our method to a comprehensive dataset of human single-unit recordings, we demonstrate that our algorithm can substantially increase the data quality of these recordings. Given our findings, we argue that future studies of single-unit activity recorded under noisy conditions should employ algorithms of this kind to improve data quality.


1982 ◽  
Vol 8 (4) ◽  
pp. 443-444 ◽  
Author(s):  
J.S. Schneider ◽  
A.A. Castaldi ◽  
T.I. Lidsky

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