Responses of vestibular nucleus neurons to inputs from the hindlimb are enhanced following a bilateral labyrinthectomy

McCall, Andrew A.; Moy, Jennifer; Puterbaugh, Sonya R.; DeMayo, William M.; Yates, Bill J.

doi:10.1152/japplphysiol.01389.2012

Cited by 10 publications

(20 citation statements)

References 51 publications

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“…Similarly, another study indicated that the responses to vestibular stimulation of neurons in the rostral ventrolateral medulla that participate in cardiovascular regulation are exaggerated in decerebrate cats (Destefino et al 2011). Other studies compared responses to whole-body rotations of neurons in the caudal vestibular nuclei in decerebrate (Endo et al 1995; Arshian et al 2013) and conscious felines (Miller et al 2008a; McCall et al 2013) and reported little difference in findings between the preparations. Hence, it appears that decerebration is more likely to unmask responses to vestibular stimulation in brain regions that receive multisynaptic inputs from the labyrinth than areas that receive inputs directly from the inner ear.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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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 (STC) 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 cast 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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Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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“…Comparisons in decerebrate and conscious cats of the effects of electrical stimulation of hindlimb nerves on vestibular nucleus neuronal activity revealed some similarities, as well as differences (238, 239). Similarities across preparations include the following: the majority of vestibular nucleus neurons received convergent limb inputs from multiple nerves; response latencies were ~20 ms suggesting that polysynaptic pathways conveyed limb inputs to vestibular nucleus neurons; most responses were excitatory; and the proportion of neurons activated by hindlimb nerve stimulation increased after bilateral labyrinthectomy (238, 239). By contrast, low-intensity stimuli [<twice threshold (T) for eliciting a compound action potential in the stimulated nerve] elicited changes in activity of many vestibular nucleus neurons in decerebrate animals, but such low-intensity stimuli were ineffective in conscious animals.…”

Section: Transformation Of Vestibular Reflexes By Descending Pathwaysmentioning

confidence: 98%

Section: Transformation Of Vestibular Reflexes By Descending Pathwaysmentioning

confidence: 99%

“…The effects of hindlimb somatosensory inputs on the activity of vestibular nucleus neurons have been studied in both decerebrate and conscious cats by the same investigators, using the same equipment and methodology during experiments in both preparations, thus permitting comparisons (75, 78, 238, 239). Comparisons in decerebrate and conscious cats of the effects of electrical stimulation of hindlimb nerves on vestibular nucleus neuronal activity revealed some similarities, as well as differences (238, 239). Similarities across preparations include the following: the majority of vestibular nucleus neurons received convergent limb inputs from multiple nerves; response latencies were ~20 ms suggesting that polysynaptic pathways conveyed limb inputs to vestibular nucleus neurons; most responses were excitatory; and the proportion of neurons activated by hindlimb nerve stimulation increased after bilateral labyrinthectomy (238, 239).…”

Section: Transformation Of Vestibular Reflexes By Descending Pathwaysmentioning

confidence: 99%

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Descending Influences on Vestibulospinal and Vestibulosympathetic Reflexes

2017

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This review considers the integration of vestibular and other signals by the central nervous system pathways that participate in balance control and blood pressure regulation, with an emphasis on how this integration may modify posture-related responses in accordance with behavioral context. Two pathways convey vestibular signals to limb motoneurons: the lateral vestibulospinal tract and reticulospinal projections. Both pathways receive direct inputs from the cerebral cortex and cerebellum, and also integrate vestibular, spinal, and other inputs. Decerebration in animals or strokes that interrupt corticobulbar projections in humans alter the gain of vestibulospinal reflexes and the responses of vestibular nucleus neurons to particular stimuli. This evidence shows that supratentorial regions modify the activity of the vestibular system, but the functional importance of descending influences on vestibulospinal reflexes acting on the limbs is currently unknown. It is often overlooked that the vestibulospinal and reticulospinal systems mainly terminate on spinal interneurons, and not directly on motoneurons, yet little is known about the transformation of vestibular signals that occurs in the spinal cord. Unexpected changes in body position that elicit vestibulospinal reflexes can also produce vestibulosympathetic responses that serve to maintain stable blood pressure. Vestibulosympathetic reflexes are mediated, at least in part, through a specialized group of reticulospinal neurons in the rostral ventrolateral medulla that project to sympathetic preganglionic neurons in the spinal cord. However, other pathways may also contribute to these responses, including those that dually participate in motor control and regulation of sympathetic nervous system activity. Vestibulosympathetic reflexes differ in conscious and decerebrate animals, indicating that supratentorial regions alter these responses. However, as with vestibular reflexes acting on the limbs, little is known about the physiological significance of descending control of vestibulosympathetic pathways.

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“…Several physiologic studies provide evidence supporting this hypothesis. VN neurons respond to electrical stimulation of hindlimb nerves (Wilson et al 1966; Jian et al 2002; McCall et al 2013) and the activity of VN neurons in decerebrate felines is modulated during hindlimb movement (Fredrickson et al 1966; Orlovsky 1972; Arshian et al 2014), with most VN neurons encoding the direction of hindlimb movement (Arshian et al 2014). …”

Section: Introductionmentioning

confidence: 99%

Hindlimb movement modulates the activity of rostral fastigial nucleus neurons that process vestibular input

et al. 2015

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Integration of vestibular and proprioceptive afferent information within the central nervous system is a critical component of postural regulation. We recently demonstrated that labyrinthine and hindlimb signals converge onto vestibular nucleus neurons, such that hindlimb movement modulates the activity of these cells. However, it is unclear whether similar convergence of hindlimb and vestibular signals also occurs upstream from the vestibular nuclei, particularly in the rostral fastigial nucleus (rFN). We tested the hypothesis that rFN neurons have similar responses to hindlimb movement as vestibular nucleus neurons. Recordings were obtained from 53 rFN neurons that responded to hindlimb movement in decerebrate cats. In contrast to vestibular nucleus neurons, which commonly encoded the direction of hindlimb movement (81% of neurons), few rFN neurons (21%) that responded to leg movement encoded such information. Instead, most rFN neurons responded to both limb flexion and extension. Half of the rFN neurons whose activity was modulated by hindlimb movement received convergent vestibular inputs. These results show that rFN neurons receive somatosensory inputs from the hindlimb, and that a subset of rFN neurons integrates vestibular and hindlimb signals. Such rFN neurons likely perform computations that participate in maintenance of balance during upright stance and movement. Although vestibular nucleus neurons are interconnected with the rFN, the dissimilarity of responses of neurons sensitive to hindlimb movement in the two regions suggest that they play different roles in coordinating postural responses during locomotion and other movements which entail changes in limb position.

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Responses of vestibular nucleus neurons to inputs from the hindlimb are enhanced following a bilateral labyrinthectomy

Cited by 10 publications

References 51 publications

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

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

Descending Influences on Vestibulospinal and Vestibulosympathetic Reflexes

Hindlimb movement modulates the activity of rostral fastigial nucleus neurons that process vestibular input

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