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

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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.

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References

  • Anderson JH, Blanks RHI, Precht W (1978) Response characteristics of semicircular canal and otolith systems in the cat. I. Dynamic responses of primary vestibular fibers. Exp Brain Res 32:491–507

    PubMed  CAS  Google Scholar 

  • Baker J, Goldberg J, Hermann G, Peterson B (1984) Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats. Brain Res 294:138–143

    Article  PubMed  CAS  Google Scholar 

  • Balaban CD (1996) Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on the autonomic nervous system. Exp Brain Res 108:367–381

    Article  PubMed  CAS  Google Scholar 

  • Balaban CD (1999) Vestibular autonomic regulation (including motion sickness and the mechanism of vomiting). Curr Opin Neurol 12:29–33

    Article  PubMed  CAS  Google Scholar 

  • Barman SM, Gebber GL (1987) Lateral tegmental field neurons of cat medulla: a source of basal activity of ventrolateral medullospinal sympathoexcitatory neurons. J Neurophysiol 57:1410–1424

    PubMed  CAS  Google Scholar 

  • Barman SM, Gebber GL, Orer HS (2000) Medullary lateral tegmental field: an important source of basal sympathetic nerve discharge in the cat. Am J Physiol Regul Integr Comp Physiol 278:R995–R1004

    PubMed  CAS  Google Scholar 

  • Barman SM, Sugiyama Y, Suzuki T, Cotter LA, DeStefino VJ, Reighard DA, Cass SP, Yates BJ (2011) Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs. Am J Physiol Regul Integr Comp Physiol 301:R937–R946

    Article  PubMed  CAS  Google Scholar 

  • Berman AI (1968) The brain stem of the cat. University of Wisconsin Press, Madison

    Google Scholar 

  • Bolton PS, Goto T, Schor RH, Wilson VJ, Yamagata Y, Yates BJ (1992) Response of pontomedullary reticulospinal neurons to vestibular stimuli in vertical planes. Role in vertical vestibulospinal reflexes of the decerebrate cat. J Neurophysiol 67:639–647

    PubMed  CAS  Google Scholar 

  • Borison HL, Wang SC (1949) Functional localization of central coordinating mechanism for emesis in cat. J Neurophysiol 12:305–313

    PubMed  CAS  Google Scholar 

  • Cheung BS, Money KE, Jacobs I (1990) Motion sickness susceptibility and aerobic fitness: a longitudinal study. Aviation Space Environ Med 61:201–204

    CAS  Google Scholar 

  • Correia MJ, Guedry FE Jr (1966) Modification of vestibular responses as a function of rate of rotation about an Earth-horizontal axis. Acta Otolaryngol 62:297–308

    Article  PubMed  CAS  Google Scholar 

  • DeStefino VJ, Reighard DA, Sugiyama Y, Suzuki T, Cotter LA, Larson MG, Gandhi NJ, Barman SM, Yates BJ (2011) Responses of neurons in the rostral ventrolateral medulla (RVLM) to whole-body rotations: comparisons in decerebrate and conscious cats. J Appl Physiol 110:1699–1707

    Article  PubMed  CAS  Google Scholar 

  • Fernandez C, Goldberg JM (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661–675

    PubMed  CAS  Google Scholar 

  • Fernandez C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996–1008

    PubMed  CAS  Google Scholar 

  • Fukuda H, Koga T (1991) The Botzinger complex as the pattern generator for retching and vomiting in the dog. Neurosci Res 12:471–485

    Article  PubMed  CAS  Google Scholar 

  • Fukuda H, Koga T (1992) Non-respiratory neurons in the Botzinger complex exhibiting appropriate firing patterns to generate the emetic act in dogs. Neurosci Res 14:180–194

    Article  PubMed  CAS  Google Scholar 

  • Golding JF (2006) Motion sickness susceptibility. Auton Neurosci 129:67–76

    Article  PubMed  Google Scholar 

  • Guedry FE Jr (1965) Orientation of the rotation-axis relative to gravity: its influence on nystagmus and the sensation of rotation. Acta Otolaryngol 60:30–48

    Article  PubMed  Google Scholar 

  • Herbert H, Moga MM, Saper CB (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 293:540–580

    Article  PubMed  CAS  Google Scholar 

  • Kasper J, Schor RH, Wilson VJ (1988) Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation. J Neurophysiol 60:1753–1764

    PubMed  CAS  Google Scholar 

  • Koga T, Qu R, Fukuda H (1998) The central pattern generator for vomiting may exist in the reticular area dorsomedial to the retrofacial nucleus in dogs. Exp Brain Res 118:139–147

    Article  PubMed  CAS  Google Scholar 

  • Miller AD, Wilson VJ (1983) Vestibular-induced vomiting after vestibulocerebellar lesions. Brain Behav Evol 23:26–31

    Article  PubMed  CAS  Google Scholar 

  • Miller AD, Nonaka S, Jakus J (1994) Brain areas essential or non-essential for emesis. Brain Res 647:255–264

    Article  PubMed  CAS  Google Scholar 

  • Miller DM, Cotter LA, Gandhi NJ, Schor RH, Cass SP, Huff NO, Raj SG, Shulman JA, Yates BJ (2008a) Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy. Exp Brain Res 188:175–186

    Article  PubMed  CAS  Google Scholar 

  • Miller DM, Cotter LA, Gandhi NJ, Schor RH, Huff NO, Raj SG, Shulman JA, Yates BJ (2008b) Responses of rostral fastigial nucleus neurons of conscious cats to rotations in vertical planes. Neuroscience 155:317–325

    Article  PubMed  CAS  Google Scholar 

  • Money KE (1970) Motion sickness. Physiol Rev 50:1–39

    PubMed  CAS  Google Scholar 

  • Moy JD, Miller DJ, Catanzaro MF, Boyle BM, Ogburn SW, Cotter LA, Yates BJ, McCall AA (2012) Responses of neurons in the caudal medullary lateral tegmental field to visceral inputs and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 303:R929–R940

    Article  PubMed  CAS  Google Scholar 

  • Orer HS, Barman SM, Gebber GL, Sykes SM (1999) Medullary lateral tegmental field: an important synaptic relay in the baroreceptor reflex pathway of the cat. Am J Physiol 277:R1462–R1475

    PubMed  CAS  Google Scholar 

  • Orer HS, Gebber GL, Phillips SW, Barman SM (2004) Role of the medullary lateral tegmental field in reflex-mediated sympathoexcitation in cats. Am J Physiol Regul Integr Comp Physiol 286:R451–R464

    Article  PubMed  CAS  Google Scholar 

  • Reason JT (1978) Motion sickness adaptation: a neural mismatch model. J R Soc Med 71:819–829

    PubMed  CAS  Google Scholar 

  • Schor RH, Angelaki DE (1992) The algebra of neural response vectors. Ann New York Acad Sci 656:190–204

    Article  CAS  Google Scholar 

  • Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146

    PubMed  CAS  Google Scholar 

  • Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res 142:439–462

    Article  PubMed  Google Scholar 

  • Sugiyama Y, Suzuki T, Destefino VJ, Yates BJ (2011) Integrative responses of neurons in nucleus tractus solitarius to visceral afferent stimulation and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 301:R1380–R1390

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Sugiyama Y, Yates BJ (2012) Integrative responses of neurons in parabrachial nuclei to a neurogenic gastrointestinal stimulus and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 302:R965–R975

    Article  PubMed  CAS  Google Scholar 

  • Wang SC, Borison HL (1951) The vomiting center; its destruction by radon implantation in dog medulla oblongata. Am J Physiol 166:712–717

    PubMed  CAS  Google Scholar 

  • Yates BJ (2009) Motion sickness. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, Heidelberg, pp 2410–2413

    Chapter  Google Scholar 

  • Yates BJ, Balaban CD, Miller AD, Endo K, Yamaguchi Y (1995) Vestibular inputs to the lateral tegmental field of the cat: potential role in autonomic control. Brain Res 689:197–206

    Article  PubMed  CAS  Google Scholar 

  • Yates BJ, Miller AD, Lucot JB (1998) Physiological basis and pharmacology of motion sickness: an update. Brain Res Bull 47:395–406

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Lucy Cotter for technical assistance. Funding was provided by Grant R01-DC003732 from the National Institutes of Health (USA).

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Correspondence to Bill J. Yates.

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McCall, A.A., Moy, J.D., DeMayo, W.M. et al. Processing of vestibular inputs by the medullary lateral tegmental field of conscious cats: implications for generation of motion sickness. Exp Brain Res 225, 349–359 (2013). https://doi.org/10.1007/s00221-012-3376-1

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  • DOI: https://doi.org/10.1007/s00221-012-3376-1

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