Processing of vestibular inputs by the medullary lateral tegmental field of conscious cats: implications for generation of motion sickness

Abstract

The dorsolateral reticular formation of the caudal medulla, the lateral tegmental field (LTF), participates in generating vomiting. LTF neurons exhibited complex responses to vestibular stimulation in decerebrate cats, indicating that they received converging inputs from a variety of labyrinthine receptors. Such a convergence pattern of vestibular inputs is appropriate for a brain region that participates in generating motion sickness. Since responses of brainstem neurons to vestibular stimulation can differ between decerebrate and conscious animals, the current study examined the effects of whole-body rotations in vertical planes on the activity of LTF neurons in conscious felines. Wobble stimuli, fixed-amplitude tilts, the direction of which moves around the animal at a constant speed, were used to determine the response vector orientation, and also to ascertain whether neurons had spatial–temporal convergence (STC) behavior (which is due to the convergence of vestibular inputs with different spatial and temporal properties). The proportion of LTF neurons with STC behavior in conscious animals (25 %) was similar to that in decerebrate cats. Far fewer neurons in other regions of the feline brainstem had STC behavior, confirming findings that many LTF neurons receive converging inputs from a variety of labyrinthine receptors. However, responses to vertical plane vestibular stimulation were considerably different in decerebrate and conscious felines for LTF neurons lacking STC behavior. In decerebrate cats, most LTF neurons had graviceptive responses to rotations, similar to those of otolith organ afferents. However, in conscious animals, the response properties were similar to those of semicircular canal afferents. These differences show that higher centers of the brain that are removed during decerebration regulate the labyrinthine inputs relayed to the LTF, either by gating connections in the brainstem or by conveying vestibular inputs directly to the region.

Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats

“…Fos-ir neurons activated by sinusoidal horizontal rotations were first observed at P4 in several reticular areas that are involved in modulating vestibulo-spinal (Bolton et al 1992;Peterson et al 1980) and autonomic functions (McCall et al 2013;Mori et al 2001): gigantocellular reticular nucleus (Gi) and dorsal paragigantocellular reticular nucleus (DPGi). The number of Fos-ir neurons in these reticular nuclei increased towards the end of the third postnatal week and maintained high in adulthood (Fig.…”

“…Furthermore, medullary reticulospinal neurons were found to regulate vestibulo-respiratory responses (Mori et al 2001). More recently, medullary reticular neurons responding to vertical rotations were also found to be involved in the generation of motion sickness (McCall et al 2013).…”

Integration of vestibular and emetic gastrointestinal signals that produce nausea and vomiting: potential contributions to motion sickness

“…Studies in decerebrate and conscious cats indicated that the responses of many LTF neurons to whole-body rotations in vertical planes are highly complex, and do not reflect a simple integration of signals from otolith organs and semicircular canals (Moy et al 2012; McCall et al. 2013).…”

“…The fraction of neurons with STC responses has been determined in conscious cats for three brainstem areas that participate in generating nausea and vomiting: LTF (McCall et al 2013), the caudal aspect of the vestibular nuclei (Miller et al 2008a), and the rostral fastigial nucleus (Miller et al 2008b). Less than 10% of neurons in the rostral fastigial and caudal vestibular nuclei of conscious cats exhibited STC responses, whereas 25% of neurons in the LTF had such complex responses to vestibular stimulation.…”

“…Abbreviations : CED , contralateral ear-down roll; IED , ipsilateral ear-down roll; ND , nose-down pitch; NU , nose-up pitch. Adapted from (McCall et al 2013). …”