Coding of Velocity Storage in the Vestibular Nuclei

Yakushin, Sergei B.; Raphan, Theodore; Cohen, Bernard

doi:10.3389/fneur.2017.00386

Cited by 53 publications

(55 citation statements)

References 95 publications

(171 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Neuronal circuitry subserving the VSM has been postulated to lie within the brainstem vestibular nuclei 42 . A subgroup of neurons in the medial and superior vestibular nuclei in monkeys showed highly correlated firing modulation with OKAN eye velocity [43][44][45] . Electrical stimulation in this area modulate the VSM 46 while midline sections of the commissural connection between bilateral vestibular nuclei abolished velocity storage capability 47 .…”

Section: Discussionmentioning

confidence: 99%

Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Miki

Urase

Baker

et al. 2020

Sci Rep

View full text Add to dashboard Cite

predictive motor control is ubiquitously employed in animal kingdom to achieve rapid and precise motor action. in most vertebrates large, moving visual scenes induce an optokinetic response (oKR) control of eye movements to stabilize vision. In goldfish, the OKR was found to be predictive after a prolonged exposure to temporally periodic visual motion. A recent study showed the cerebellum necessary to acquire this predictive OKR (pOKR), but it remained unclear as to whether the cerebellum alone was sufficient. Herein we examined different fish species known to share the basic architecture of cerebellar neuronal circuitry for their ability to acquire pOKR. Carps were shown to acquire pOKR like goldfish while zebrafish and medaka did not, demonstrating the cerebellum alone not to be sufficient. Interestingly, those fish that acquired pOKR were found to exhibit long-lasting optokinetic after nystagmus (OKAN) as opposed to those that didn't. To directly manipulate OKAN vestibularneurectomy was performed in goldfish that severely shortened OKAN, but pOKR was acquired comparable to normal animals. these results suggest that the neuronal circuitry producing oKAn, known as the velocity storage mechanism (VSM), is required to acquire pOKR irrespective of OKAN duration. Taken together, we conclude that pOKR is acquired through recurrent cerebellum-brainstem parallel loops in which the cerebellum adjusts VSM signal flow and, in turn, receives appropriately timed eye velocity information to clock visual world motion.

show abstract

Section: Discussionmentioning

confidence: 99%

Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Miki

Urase

Baker

et al. 2020

Sci Rep

View full text Add to dashboard Cite

show abstract

“…It should be noted that vestibular‐only and vestibular‐plus‐saccade neurons encode indirectly a slow component of vestibulo‐ocular reflex (VOR) via velocity storage mechanism (Reisine and Raphan ; Yakushin et al. ), while a direct pathway of VOR is coded by position‐vestibular‐pause and eye‐head velocity neurons (Fuchs and Kimm ; Scudder and Fuchs ). It is shown that the adaptation of linear and angular VORs is specific to head orientation relative to gravity (Shelhamer et al.…”

Section: Discussionmentioning

confidence: 99%

“…We suggest that main role of STC processing in canal-otolith neurons is a link of two coordinate systems within the vestibular system, namely: external system (i.e., accelerations in spatial coordinates) and internal system (i.e., rotations in head coordinates); and the damage of STC processing could initiates difficulties in coding of vestibulo-motor reactions at the level of brain stem and follow-up difficulties or disorder in encoding of spatial orientation, perception, and spatial memory implemented at other brain levels/structures. It should be noted that vestibular-only and vestibular-plus-saccade neurons encode indirectly a slow component of vestibulo-ocular reflex (VOR) via velocity storage mechanism (Reisine and Raphan 1992;Yakushin et al 2017), while a direct pathway of VOR is coded by position-vestibular-pause and eye-head velocity neurons (Fuchs and Kimm 1975;Scudder and Fuchs 1992). It is shown that the adaptation of linear and angular VORs is specific to head orientation relative to gravity (Shelhamer et al 2002;Yakushin et al 2003aYakushin et al ,b, 2005b.…”

Section: Discussionmentioning

confidence: 99%

Adaptation of spatio-temporal convergent properties in central vestibular neurons in monkeys

et al. 2018

Self Cite

View full text Add to dashboard Cite

The spatio‐temporal convergent (STC) response occurs in central vestibular cells when dynamic and static inputs are activated. The functional significance of STC behavior is not fully understood. Whether STC is a property of some specific central vestibular neurons, or whether it is a response that can be induced in any neuron at some frequencies is unknown. It is also unknown how the change in orientation of otolith polarization vector (orientation adaptation) affects STC behavior. A new complex model, that includes inputs with regular and irregular discharges from both canal and otolith afferents, was applied to experimental data to determine how many convergent inputs are sufficient to explain the STC behavior as a function of frequency and orientation adaptation. The canal–otolith and otolith‐only neurons were recorded in the vestibular nuclei of three monkeys. About 42% (11/26 canal–otolith and 3/7 otolith‐only) neurons showed typical STC responses at least at one frequency before orientation adaptation. After orientation adaptation in side‐down head position for 2 h, some canal–otolith and otolith‐only neurons altered their STC responses. Thus, STC is a property of weights of the regular and irregular vestibular afferent inputs to central vestibular neurons which appear and/or disappear based on stimulus frequency and orientation adaptation. This indicates that STC properties are more common for central vestibular neurons than previously assumed. While gravity‐dependent adaptation is also critically dependent on stimulus frequency and orientation adaptation, we propose that STC behavior is also linked to the neural network responsible for localized contextual learning during gravity‐dependent adaptation.

show abstract

“…Based on new findings from a three-dimensional study of the characteristics of vestibular-only (VO) neurons in the medial and superior vestibular nuclei ( 40 ), it is proposed that there is a similar situation that produces the MdDS, namely, oscillation between the VO neuronal groups on each side of the brainstem at frequencies of 0.2 or 0.3 Hz, controlled by output from the cerebellar nodulus that produces the MdDS.…”

Section: Mdds Generation Hypothesismentioning

confidence: 99%

“…If such an arrangement exists, these neural groups should have substantial connections between them that could monitor and maintain the oscillations. The VO neurons characteristically have a time constant during rotation of 15–25 s ( 40 , 41 ), but these neurons are capable of responding at a much faster rate, i.e., up to 450 impulses/s ( 42 , 43 ). As suggested earlier, there should be adaptable elements in these structures to account for the proposed shift in the pitch orientation vector that drives them into oscillation when confronted with exposure to head roll on the sea or in the air.…”

Section: Relevant Questionsmentioning

confidence: 99%

Hypothesis: The Vestibular and Cerebellar Basis of the Mal de Debarquement Syndrome

2018

Self Cite

View full text Add to dashboard Cite

The Mal de Debarquement syndrome (MdDS) generally follows sea voyages, but it can occur after turbulent flights or spontaneously. The primary features are objective or perceived continuous rocking, swaying, and/or bobbing at 0.2 Hz after sea voyages or 0.3 Hz after flights. The oscillations can continue for months or years and are immensely disturbing. Associated symptoms appear to be secondary to the incessant sensation of movement. We previously suggested that the illness can be attributed to maladaptation of the velocity storage integrator in the vestibular system, but the actual neural mechanisms driving the MdDS are unknown. Here, based on experiments in subhuman primates, we propose a series of postulates through which the MdDS is generated: (1) The MdDS is produced in the velocity storage integrator by activation of vestibular-only (VO) neurons on either side of the brainstem that are oscillating back and forth at 0.2 or 0.3 Hz. (2) The groups of VO neurons are driven by signals that originate in Purkinje cells in the cerebellar nodulus. (3) Prolonged exposure to roll, either on the sea or in the air, conditions the roll-related neurons in the nodulus. (4) The prolonged exposure causes a shift of the pitch orientation vector from its original position aligned with gravity to a position tilted in roll. (5) Successful treatment involves exposure to a full-field optokinetic stimulus rotating around the spatial vertical countering the direction of the vestibular imbalance. This is done while rolling the head at the frequency of the perceived rocking, swaying, or bobbing. We also note experiments that could be used to verify these postulates, as well as considering potential flaws in the logic. Important unanswered questions: (1) Why does the MdDS predominantly affect women? (2) What aspect of roll causes the prolongation of the tilted orientation vector, and why is it so prolonged in some individuals? (3) What produces the increase in symptoms of some patients when returning home after treatment, and how can this be avoided? We also posit that the same mechanisms underlie the less troublesome and shorter duration Mal de Debarquement.

show abstract

Coding of Velocity Storage in the Vestibular Nuclei

Cited by 53 publications

References 95 publications

Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Adaptation of spatio-temporal convergent properties in central vestibular neurons in monkeys

Hypothesis: The Vestibular and Cerebellar Basis of the Mal de Debarquement Syndrome

Contact Info

Product

Resources

About