Evidence for vestibular regulation of autonomic functions in a mouse genetic model

Murakami, Dean M.; Erkman, Linda; Hermanson, Ola; Rosenfeld, Michael G.; Fuller, Charles A.

doi:10.1073/pnas.252652299

Cited by 43 publications

(48 citation statements)

References 42 publications

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“…The result is an increased level of tonic vestibular discharge and in turn increased levels of activity in central vestibular relays (Fuller et al , 2004Kaufman et al 1992;Murakami et al 2002). Similar changes have been reported during space flight with increases and decreases in gravitational loading (Pompeiano et al 2001a, b).…”

Section: Discharge Rates and The Unloaded Maculasupporting

confidence: 60%

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Resting Discharge Patterns of Macular Primary Afferents in Otoconia-Deficient Mice

Jones

Hoffman³

2008

JARO

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Vestibular primary afferents in the normal mammal are spontaneously active. The consensus hypothesis states that such discharge patterns are independent of stimulation and depend instead on excitation by vestibular hair cells due to background release of synaptic neurotransmitter. In the case of otoconial sensory receptors, it is difficult to test the independence of resting discharge from natural tonic stimulation by gravity. We examined this question by studying discharge patterns of single vestibular primary afferent neurons in the absence of gravity stimulation using two mutant strains of mice that lack otoconia (OTO−; head tilt, het-Nox3, and tilted, tlt-Otop1). Our findings demonstrated that macular primary afferent neurons exhibit robust resting discharge activity in OTO− mice. Spike interval coefficient of variation (CV=SD/mean spike interval) values reflected both regular and irregular discharge patterns in OTO− mice, and the range of values for rate-normalized CV was similar to mice and other mammals with intact otoconia although there were proportionately fewer irregular fibers. Mean discharge rates were slightly higher in otoconia-deficient strains even after accounting for proportionately fewer irregular fibers [OTO−=75.4±31.1(113) vs OTO+=68.1±28.5(143) in sp/s]. These results confirm the hypothesis that resting activity in macular primary afferents occurs in the absence of ambient stimulation. The robust discharge rates are interesting in that they may reflect the presence of a functionally 'up-regulated' tonic excitatory process in the absence of natural sensory stimulation.

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Section: Discharge Rates and The Unloaded Maculasupporting

confidence: 60%

“…A swimming test (Jones et al 1999;Lim et al 1978;Ornitz et al 1998) was performed on each animal immediately prior to experiments. Normal swimming behavior was represented by the animal's ability to orient in a head-up position and swim comfortably.…”

Section: Animals and Surgical Preparationmentioning

confidence: 99%

Resting Discharge Patterns of Macular Primary Afferents in Otoconia-Deficient Mice

Jones

Hoffman³

2008

JARO

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“…Any inconsistency may be due to variable autonomic tone during electrocardiography in the previous studies; autonomic nervous activity was evaluated only in one [6]. Sympathetic activation through hearing stimuli is absent in SNHL children [22,23]. In our study, the sympathetic activity of the SHNL group may therefore be less than that in the control group, as evidenced by the decreased nLFP and lower RRI in the SNHL group (Table 1).…”

Section: Discussionmentioning

confidence: 64%

Effects of sevoflurane on QT parameters in children with congenital sensorineural hearing loss

Kim

et al. 2008

Anaesthesia

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SummarySevoflurane prolongs the QT interval (QTI). Patients with congenital sensorineural hearing loss (SNHL) often have a prolonged QTI. This study was to investigate the effects of sevoflurane on the QTI in SNHL and control children. Thirty patients with SNHL and 30 controls were studied. The corrected QT interval (QTc), interval from peak to end of T wave (Tp-e) and QT variability index (QTVI) were analysed. QTc and Tp-e were estimated by the average QTc and Tp-e measured beat-by-beat for 15 min. Heart rate power spectral analysis was performed. In both groups, QTc and QTVI increased during anaesthesia, but Tp-e did not change. There were no differences in QTc, QTVI, Tp-e, low-and high-frequency power between the two groups. In both groups, sevoflurane lengthened the QTc and QTVI intervals but not Tp-e. Sevoflurane is a popular inhalational agent for general anaesthesia. It blocks the slowly activating delayed rectifier K current (I Ks ) and prolongs the QT interval in both children [1,2] and adults [3,4]. Such changes may be of clinical significance in patients presenting with long QT syndrome, hypokalaemia or in the presence of other agents or factors that lengthen the QT interval.The Jervell and Lange-Nielson syndrome [5] is a long-QT syndrome found among patients with congenital sensorineural hearing loss (SNHL). The deafness is attributed to mutations on the KCNQ1 or KCNE1 genes encoding the rapidly activating delayed rectifier K + channel (I Kr ) in the inner ear. Similar mutations, present in the cardiomyocyte, cause the long QT syndrome. However, it was reported that even patients with congenital SNHL who do not meet the criteria for Jervell and Lange-Nielsen syndrome have increased QTc [6,7]. Thus such children may be at increased risk of corrected QT (QTc) prolongation during sevoflurane anaesthesia.The aim of this study was to investigate how sevoflurane changes the QT parameters in children with congenital SNHL, and whether this differs from the changes in normal children produced by sevoflurane.The QT parameters we analysed were QTc, interval from peak to end of T wave (Tp-e) and QT variability index (QTVI) which reflect the action potential duration of the ventricle, transmural repolarisation dispersion in the action potential duration [8,9] and temporal repolarisation lability [10], respectively. The clinical importance of increases in QT parameter values lies in their association with malignant ventricular arrhythmias [11][12][13]. To improve the accuracy of the average of QTc and Tp-e, we averaged all beat-by-beat QTc and Tp-e values measured automatically over the 15 min period, as well as four manually measured values of QTc and Tp-e. Methods Study populationAfter obtaining approval from the institutional ethics committee of the hospital and written informed consent from parents or guardians, the study was performed on 30 children with congenital SNHL (SNHL group) and 30 patients with chronic otitis media (control group), both of whom required ear surgery and were aged between 2 and 15 year...

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confidence: 99%

“…The vestibular system is primarily involved in gaze stabilization and postural control (23), but its influence has been expanded to autonomic and bone regulation (11,61,63), spatial learning and memory (5,6,56), and spatial orientation and perception of gravitational verticality (37). Studies carried out in environments in which gravity is altered have shown evidence of a possible influence of the vestibular system on hypothalamic circadian function in rats (27) and mice (18,46); disruption of circadian rhythms of temperature (Temp) and locomotor activity (Act) have been similarly observed in both species for about 7 days in a 2 G environment generated by a centrifuge. Knockout mice devoid of otolithic vestibular sensors [het(Ϫ/Ϫ) mice] remained unaffected by hypergravity at 2 G (18).…”

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confidence: 99%

Vestibular loss disrupts daily rhythm in rats

Martin

Mauvieux

Bulla

et al. 2015

Journal of Applied Physiology

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Hypergravity disrupts the circadian regulation of temperature (Temp) and locomotor activity (Act) mediated through the vestibular otolithic system in mice. In contrast, we do not know whether the anatomical structures associated with vestibular input are crucial for circadian rhythm regulation at 1 G on Earth. In the present study we observed the effects of bilateral vestibular loss (BVL) on the daily rhythms of Temp and Act in semipigmented rats. Our model of vestibular lesion allowed for selective peripheral hair cell degeneration without any other damage. Rats with BVL exhibited a disruption in their daily rhythms (Temp and Act), which were replaced by a main ultradian period ( Ͻ20 h) for 115.8 Ϯ 68.6 h after vestibular lesion compared with rats in the control group. Daily rhythms of Temp and Act in rats with BVL recovered within 1 wk, probably counterbalanced by photic and other nonphotic time cues. No correlation was found between Temp and Act daily rhythms after vestibular lesion in rats with BVL, suggesting a direct influence of vestibular input on the suprachiasmatic nucleus. Our findings support the hypothesis that the vestibular system has an influence on daily rhythm homeostasis in semipigmented rats on Earth, and raise the question of whether daily rhythms might be altered due to vestibular pathology in humans. vestibular system; biological rhythms; temperature; locomotor activity; rats LOCATED IN THE TEMPORAL BONES, the vestibular system is composed of three semicircular canals that encode head rotation velocity and two otolithic macula that encode linear acceleration and gravity force. The vestibular system is primarily involved in gaze stabilization and postural control (23), but its influence has been expanded to autonomic and bone regulation (11,61,63), spatial learning and memory (5, 6, 56), and spatial orientation and perception of gravitational verticality (37). Studies carried out in environments in which gravity is altered have shown evidence of a possible influence of the vestibular system on hypothalamic circadian function in rats (27) and mice (18,46

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Evidence for vestibular regulation of autonomic functions in a mouse genetic model

Abstract: circadian rhythm ͉ gravity ͉ temperature regulation ͉ Brn-3.1 ͉ parabrachial

Cited by 43 publications

References 42 publications

Resting Discharge Patterns of Macular Primary Afferents in Otoconia-Deficient Mice

Resting Discharge Patterns of Macular Primary Afferents in Otoconia-Deficient Mice

Effects of sevoflurane on QT parameters in children with congenital sensorineural hearing loss

Vestibular loss disrupts daily rhythm in rats

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