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Integration of vestibular and gastrointestinal inputs by cerebellar fastigial nucleus neurons: multisensory influences on motion sickness

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Abstract

Previous studies demonstrated that ingestion of the emetic compound copper sulfate (CuSO4) alters the responses to vestibular stimulation of a large fraction of neurons in brainstem regions that mediate nausea and vomiting, thereby affecting motion sickness susceptibility. Other studies suggested that the processing of vestibular inputs by cerebellar neurons plays a critical role in generating motion sickness and that neurons in the cerebellar fastigial nucleus receive visceral inputs. These findings raised the hypothesis that stimulation of gastrointestinal receptors by a nauseogenic compound affects the processing of labyrinthine signals by fastigial nucleus neurons. We tested this hypothesis in decerebrate cats by determining the effects of intragastric injection of CuSO4 on the responses of rostral fastigial nucleus to whole-body rotations that activate labyrinthine receptors. Responses to vestibular stimulation of fastigial nucleus neurons were more complex in decerebrate cats than reported previously in conscious felines. In particular, spatiotemporal convergence responses, which reflect the convergence of vestibular inputs with different spatial and temporal properties, were more common in decerebrate than in conscious felines. The firing rate of a small percentage of fastigial nucleus neurons (15 %) was altered over 50 % by the administration of CuSO4; the firing rate of the majority of these cells decreased. The responses to vestibular stimulation of a majority of these cells were attenuated after the compound was provided. Although these data support our hypothesis, the low fraction of fastigial nucleus neurons whose firing rate and responses to vestibular stimulation were affected by the administration of CuSO4 casts doubt on the notion that nauseogenic visceral inputs modulate motion sickness susceptibility principally through neural pathways that include the cerebellar fastigial nucleus. Instead, it appears that convergence of gastrointestinal and vestibular inputs occurs mainly in the brainstem.

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Acknowledgments

The authors thank Danielle Akinsanmi, George Bourdages, Bret Boyle, Alex Carter, Valerie Casuccio, Thomas Cooper, Bryant Fischer, and Nevin Sastry for technical assistance. Funding was provided by Grant R01-DC003732 from the National Institutes of Health (USA). Michael F. Catanzaro was supported by an American Physiological Society Undergraduate Research Excellence Fellowship.

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Authors and Affiliations

  1. Department of Otolaryngology, University of Pittsburgh, Room 519, Eye and Ear Institute, Pittsburgh, PA, 15213, USA

    Michael F. Catanzaro, Daniel J. Miller, Lucy A. Cotter, Andrew A. McCall & Bill J. Yates

  2. Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA, 15213, USA

    Michael F. Catanzaro, Daniel J. Miller & Bill J. Yates

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  1. Michael F. Catanzaro
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  2. Daniel J. Miller
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Correspondence to Bill J. Yates.

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Catanzaro, M.F., Miller, D.J., Cotter, L.A. et al. Integration of vestibular and gastrointestinal inputs by cerebellar fastigial nucleus neurons: multisensory influences on motion sickness. Exp Brain Res 232, 2581–2589 (2014). https://doi.org/10.1007/s00221-014-3898-9

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  • DOI: https://doi.org/10.1007/s00221-014-3898-9

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