Vestibular afferents to the dorsal vagal complex: substrate for vestibular-autonomic interactions in the rat

Ruggiero, David A.; Mtui, Estomih; Otake, Kazuyoshi; Anwar, Mumtaz Ali

doi:10.1016/s0006-8993(96)01099-2

Cited by 47 publications

(34 citation statements)

References 21 publications

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“…The vestibular nuclei provide direct inputs to the RVLM (28,35), as well as indirect inputs relayed through brain stem regions that mediate the baroreceptor reflex and participate in generating rhythmic SNA, including nucleus tractus solitarius (1,37,41), the lateral tegmental field (40), and the caudal ventrolateral medulla (38). One explanation for the reduced RVLM neuronal activity after the elimination of labyrinthine inputs is a loss of excitatory monosynaptic and polysynaptic excitatory drive to RVLM neurons from the vestibular nuclei.…”

Section: Discussionmentioning

confidence: 99%

Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

Barman

Sugiyama²,

Suzuki³

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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-Although it is well established that bulbospinal neurons located in the rostral ventrolateral medulla (RVLM) play a pivotal role in regulating sympathetic nerve activity and blood pressure, virtually all neurophysiological studies of this region have been conducted in anesthetized or decerebrate animals. In the present study, we used time-and frequency-domain analyses to characterize the naturally occurring discharges of RVLM neurons in conscious cats. Specifically, we compared their activity to fluctuations in carotid artery blood flow to identify neurons with cardiac-related (CR) activity; we then considered whether neurons with CR activity also had a higher-frequency rhythmic firing pattern. In addition, we ascertained whether the surgical removal of vestibular inputs altered the rhythmic discharge properties of RVLM neurons. Less than 10% of RVLM neurons expressed CR activity, although the likelihood of observing a neuron with CR activity in the RVLM varied between recording sessions, even when tracking occurred in a very limited area and was higher after vestibular inputs were surgically removed. Either a 10-Hz or a 20-to 30-Hz rhythmic discharge pattern coexisted with the CR discharges in some of the RVLM neurons. Additionally, the firing rate of RVLM neurons, including those with CR activity, decreased after vestibular lesions. These findings raise the prospect that RVLM neurons may or may not express rhythmic firing patterns at a particular time due to a variety of influences, including descending projections from higher brain centers and sensory inputs, such as those from the vestibular system. vestibular system; sympathetic nervous system; baroreceptors; 10-Hz rhythm; cardiac-related activity THERE IS A CONSENSUS THAT bulbospinal neurons located in the rostral ventrolateral medulla (RVLM) play a pivotal role in regulating the activity of sympathetic preganglionic neurons in the spinal cord that control peripheral vascular resistance and blood pressure (13,15,16). Neurophysiological studies conducted in decerebrate or anesthetized animals have characterized the firing patterns and responses to a variety of stimuli of RVLM neurons (e.g., 3, 5-7, 18, 23). A hallmark of sympathetic nerve activity (SNA) and of the activity in brain stem neurons that regulate cardiovascular function is the appearance of a cardiac-related (CR) rhythm, reflecting the influence of the baroreceptor reflex (14,20,23,25,27). In addition to the CR rhythm, several groups have noted the appearance of a 10-Hz rhythm in SNA of cats (4, 9, 10, 14, 24).We recently provided the first examples of recordings of RVLM neuronal activity in conscious animals (18). In that study, we compared in decerebrate and awake cats the responses of RVLM neurons to whole-body rotations that activate vestibular receptors. We demonstrated that RVLM neuronal responses to vestibular inputs are ordinarily suppressed in conscious animals and hypothesized that autonomic responses to a variety of inputs, including those from the inner ear, are gated by higher brai...

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Section: Discussionmentioning

confidence: 99%

Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

Barman

Sugiyama²,

Suzuki³

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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“…It is well accepted that labryrinthectomy induces compensatory changes in the neuronal architecture and function of the vestibular nuclei (7,9,49). In view of the evidence showing neural projections from the vestibular nuclei to major brain stem nuclei involved in autonomic control of HR (34,42), it is conceivable that altered neuronal function or activity in the vestibular nuclear complex of the het mice has downstream effects on the autonomic regulation of HR.…”

Section: Discussionmentioning

confidence: 99%

Diminished baroreflex control of heart rate responses in otoconia-deficient C57BL/6JEi head tilt mice

Xue

Skala

Jones

et al. 2004

American Journal of Physiology-Heart and Circulatory Physiology

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The maintenance of stable blood pressure during postural changes is known to involve integration of vestibular and cardiovascular central regulatory mechanisms. Sensory activity in the vestibular system plays an important role in cardiovascular regulation. The purpose of this study was to determine the role of vestibular gravity receptors in normal baroreflex function. Baroreflex heart rate (HR) responses to changes in blood pressure (BP) in otoconia-deficient head tilt (het) mice (n = 8) were compared with their wild-type littermates (n = 12). The study was carried out in conscious male mice chronically implanted with arterial and venous catheters for recording BP and HR and for the infusion of vasoactive drugs. Resting HR was higher in the het mice (661 +/- 13 beats/min) than in the wild-type mice (579 +/- 20 beats/min). BP was comparable in the het (113 +/- 4 mmHg) and wild-type mice (104 +/- 4 mmHg). The slopes of reflex decreases in HR in response to phenylephrine (PE) were blunted in the het mice (-5.5 +/- 1.5 beats x min(-1) x mmHg(-1)) compared with the wild-type mice (-8.5 +/- 0.9 beats x min(-1) x mmHg(-1)). Likewise, reflex tachycardic responses to decreases in BP with sodium nitroprusside (SNP) were significantly blunted in the het mice (-0.8 +/- 0.3 beats x min(-1) x mmHg(-1)) versus the wild-type mice (-2.2 +/- 0.6 beats x min(-1) x mmHg(-1)). Frequency-domain analysis of the HR variability suggests that under resting conditions, parasympathetic contribution was lower in the het versus wild-type mice. Mapping of the expression of immediate-early gene product, c-Fos, in forebrain and brain stem nuclei in response to a BP challenge showed no differences between the wild-type and het mice. These results suggest that tonic activity of gravity receptors modulates and is required for normal function of the cardiac baroreflexes.

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“…The CVN also provide considerable inputs to the cerebellar nodulus and uvula (Epema et al 1985;Sato et al 1989;Thunnissen et al 1989;Barmack et al 1992). Furthermore, the CVN project to medullary regions that participate in regulation of blood pressure and breathing (Balaban and Beryozkin 1994;Yates et al 1995;Ruggiero et al 1996;Porter and Balaban 1997;Martinelli et al 2007), and lesions of the CVN abolish cardiovascular and respiratory responses to stimulation of vestibular afferents (Uchino et al 1970;Yates et al 1993;Kerman and Yates 1998).…”

Section: Introductionmentioning

confidence: 99%

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

et al. 2008

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Although many previous experiments have considered the responses of vestibular nucleus neurons to rotations and translations of the head, little data are available regarding cells in the caudalmost portions of the vestibular nuclei (CVN), which mediate vestibulo-autonomic responses among other functions. This study examined the responses of CVN neurons of conscious cats to rotations in vertical planes, both before and after a bilateral vestibular neurectomy. None of the units included in the data sample had eye movement-related activity. In labyrinth-intact animals, some CVN neurons (22%) exhibited graviceptive responses consistent with inputs from otolith organs, but most (55%) had dynamic responses with phases synchronized with stimulus velocity. Furthermore, the large majority of CVN neurons had response vector orientations that were aligned either near the roll or vertical canal planes, and only 18% of cells were preferentially activated by pitch rotations. Sustained head-up rotations of the body provide challenges to the cardiovascular system and breathing, and thus the response dynamics of the large majority of CVN neurons were dissimilar to those of posturally-related autonomic reflexes. These data suggest that vestibular influences on autonomic control mediated by the CVN are more complex than previously envisioned, and likely involve considerable processing and integration of signals by brainstem regions involved in cardiovascular and respiratory regulation. Following a bilateral vestibular neurectomy, CVN neurons regained spontaneous activity within 24 h, and a very few neurons (<10%) responded to vertical tilts <15° in amplitude. These findings indicate that nonlabyrinthine inputs are likely important in sustaining the activity of CVN neurons; thus, these inputs may play a role in functional recovery following peripheral vestibular lesions.

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Vestibular afferents to the dorsal vagal complex: substrate for vestibular-autonomic interactions in the rat

Cited by 47 publications

References 21 publications

Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

Diminished baroreflex control of heart rate responses in otoconia-deficient C57BL/6JEi head tilt mice

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

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