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

Abstract

-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...

Vestibulo‐Sympathetic Responses

“…The RVLM also provides a major pathway through which vestibular signals are conveyed to sympathetic preganglionic neurons in the spinal cord, as indicated by the observation that bilateral chemical lesions of the RVLM abolished VSR (328). In conscious cats, a significantly higher fraction of RVLM neurons exhibited cardiac-related activity, or rhythmic bursts of action potentials synchronized with the cardiac cycle, after removal of vestibular inputs (27). In addition, a bilateral labyrinthectomy resulted in a significant reduction in the spontaneous activity of RVLM neurons, including those with cardiac related activity (27).…”

Additive Role of the Vestibular End Organ and Baroreceptors on the Regulation of Blood Pressure in Rats

“…A direct vestibular projection to the RVLM region has also been reported [18]. A series of studies by Yates and co-workers [19-21] demonstrated that signals coming from peripheral vestibular organs via the vestibular nucleus affect blood pressure, perhaps through the classic pathway of cardiovascular regulation. Electrophysiological and morphological studies have also shown that the RVLM is a key area in the pathway conveying vestibular signals to the gray substance in the spinal cord.…”

Descending Influences on Vestibulospinal and Vestibulosympathetic Reflexes

“…It has been suggested that higher brain areas adjust the responsiveness of neurons in the vestibulosympathetic reflex pathway to vestibular inputs, so that the gain of the vestibulosympathetic reflex is appropriate for the ensuing movement or postural change (32). Recordings from conscious animals also provided evidence that following a bilateral labyrinthectomy, the gain of the baroreceptor reflex is adjusted by descending signals from supratentorial brain regions (251). As noted above, a number of supratentorial regions provide inputs to neurons that comprise the vestibulosympathetic reflex pathway, and it is unclear which of these regions participates in adjusting the response gain, and where along the pathway (vestibular nuclei, NTS, CVLM, RVLM) the gain adjustments occur.…”

“…Neurophysiologic experiments on neurons that constitute vestibulosympathetic pathways are in their infancy, and just two studies (184, 251) have monitored in conscious animals the activity of RVLM neurons that play a key role in regulating sympathetic nervous system activity. Little attention has been paid to the contributions of other pathways to vestibulosympathetic responses, including those originating in the medial reticular formation, raphe nuclei, and locus coeruleus that provide monosynaptic or polysynaptic inputs to both limb motoneurons and sympathetic preganglionic neurons (53–56).…”