Neurons in the pontomedullary reticular formation receive converging inputs from the hindlimb and labyrinth

Miller, Derek M.; DeMayo, William M.; Bourdages, George; Wittman, Samuel R; Yates, Bill J.; McCall, Andrew A.

doi:10.1007/s00221-017-4875-x

Cited by 13 publications

(7 citation statements)

References 58 publications

(86 reference statements)

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“…The RS neurons of the MedRF (FTM) also have multiple inputs in addition to the MLR (Steeves and Jordan, 1984; Garcia-Rill and Skinner, 1987; Bretzner and Brownstone, 2013). They are innervated by the ipsilateral SLR (Sinnamon and Stopford, 1987; Takakusaki et al, 2016), the contralateral cerebellar locomotor region (Mori et al, 1998), the PAG (Mantyh, 1983; Dampney et al, 2013), the motor cortex via corticoreticular pathways (Matsuyama et al, 2004b), as well as various sensory systems (e.g., visual, auditory, and vestibular) (Furigo et al, 2010; Miller et al, 2017). Thus locomotion may be initiated by activation of the RF directly, bypassing the MLR (Shik et al, 1966; Noga et al, 1988; Mori et al, 1998; Bretzner and Brownstone, 2013; Capelli et al, 2017) or modulated by activation of sensory or neuromodulatory inputs to the RF (Antri et al, 2008; Smetana et al, 2010; Noga and Opris, 2017a, b; Oueghlani et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Activation of Brainstem Neurons During Mesencephalic Locomotor Region-Evoked Locomotion in the Cat

Opriş

Dai

Johnson

et al. 2019

Front. Syst. Neurosci.

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The distribution of locomotor-activated neurons in the brainstem of the cat was studied by c-Fos immunohistochemistry in combination with antibody-based cellular phenotyping following electrical stimulation of the mesencephalic locomotor region (MLR) – the anatomical constituents of which remain debated today, primarily between the cuneiform (CnF) and the pedunculopontine tegmental nuclei (PPT). Effective MLR sites were co-extensive with the CnF nucleus. Animals subject to the locomotor task showed abundant Fos labeling in the CnF, parabrachial nuclei of the subcuneiform region, periaqueductal gray, locus ceruleus (LC)/subceruleus (SubC), Kölliker–Fuse, magnocellular and lateral tegmental fields, raphe, and the parapyramidal region. Labeled neurons were more abundant on the side of stimulation. In some animals, Fos-labeled cells were also observed in the ventral tegmental area, medial and intermediate vestibular nuclei, dorsal motor nucleus of the vagus, n. tractus solitarii, and retrofacial nucleus in the ventrolateral medulla. Many neurons in the reticular formation were innervated by serotonergic fibers. Numerous locomotor-activated neurons in the parabrachial nuclei and LC/SubC/Kölliker–Fuse were noradrenergic. Few cholinergic neurons within the PPT stained for Fos. In the medulla, serotonergic neurons within the parapyramidal region and the nucleus raphe magnus were positive for Fos. Control animals, not subject to locomotion, showed few Fos-labeled neurons in these areas. The current study provides positive evidence for a role for the CnF in the initiation of locomotion while providing little evidence for the participation of the PPT. The results also show that MLR-evoked locomotion involves the parallel activation of reticular and monoaminergic neurons in the pons/medulla, and provides the anatomical and functional basis for spinal monoamine release during evoked locomotion. Lastly, the results indicate that vestibular, cardiovascular, and respiratory centers are centrally activated during MLR-evoked locomotion. Altogether, the results show a complex pattern of neuromodulatory influences of brainstem neurons by electrical activation of the MLR.

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Section: Discussionmentioning

confidence: 99%

Activation of Brainstem Neurons During Mesencephalic Locomotor Region-Evoked Locomotion in the Cat

Opriş

Dai

Johnson

et al. 2019

Front. Syst. Neurosci.

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“…In other words, the responses of reticular formation neurons to limb movement in both decerebrate and conscious animals resembled those of vestibular nucleus neurons in conscious animals. No suppression of limb position signals to reticular formation neurons by supratentorial brain regions was observed (240), as noted for vestibular nucleus neurons (75). These findings raise the possibility that higher brain areas such as cerebral cortex play fundamentally different roles in regulating the activity of the vestibulospinal and reticulospinal systems, although there is no experimental evidence to suggest the nature of the differences in regulation of the two systems.…”

Section: Transformation Of Vestibular Reflexes By Descending Pathwaysmentioning

confidence: 86%

“…Similar comparisons of responses to limb movement in decerebrate and conscious cats have been performed for reticular formation neurons (240). In both preparations, the majority of responsive reticular formation neurons encoded limb movement irrespective of the direction of the movement; few encoded limb position or the direction of limb movement.…”

Section: Transformation Of Vestibular Reflexes By Descending Pathwaysmentioning

confidence: 87%

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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“…Experimental protocols were reviewed and approved by the University of Pittsburgh's Institutional Animal Care and Use Committee and conformed to the National Research Council Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC, 2011). Data were collected from four purpose-bred spayed female cats obtained from Liberty Research (Waverly, NY, USA) that were instrumented for chronic single unit recordings using procedures described in previous publications [29][30][31][32]. These procedures will be summarized succinctly in the text below.…”

Section: Methodsmentioning

confidence: 99%

Integration of vestibular and hindlimb inputs by vestibular nucleus neurons: multisensory influences on postural control

McCall

Miller

Balaban

2021

Journal of Neurophysiology

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We recently demonstrated in decerebrate and conscious cat preparations that hindlimb somatosensory inputs converge with vestibular afferent input onto neurons in multiple CNS locations that participate in balance control. While it is known that head position and limb state modulate postural reflexes, presumably through vestibulospinal and reticulospinal pathways, the combined influence of the two inputs on the activity of neurons in these brainstem regions is unknown. In the present study, we evaluated the responses of vestibular nucleus (VN) neurons to vestibular and hindlimb stimuli delivered separately and together in conscious cats. We hypothesized that VN neuronal firing during activation of vestibular and limb proprioceptive inputs would be well-fit by an additive model. Extracellular single-unit recordings were obtained from VN neurons. Sinusoidal whole-body rotation in the roll plane was used as the search stimulus. Units responding to the search stimulus were tested for their responses to 10° ramp-and-hold roll body rotation, 60° extension hindlimb movement, and both movements delivered simultaneously. Composite response histograms were fit by a model of low and high pass filtered limb and body position signals using least squares nonlinear regression. We found that VN neuronal activity during combined vestibular and hindlimb proprioceptive stimulation in the conscious cat is well-fit by a simple additive model for signals with similar temporal dynamics. The mean R2value for goodness of fit across all units was 0.74 ±0.17. It is likely that VN neurons that exhibit these integrative properties participate in adjusting vestibulospinal outflow in response to limb state.

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Neurons in the pontomedullary reticular formation receive converging inputs from the hindlimb and labyrinth

Cited by 13 publications

References 58 publications

Activation of Brainstem Neurons During Mesencephalic Locomotor Region-Evoked Locomotion in the Cat

Activation of Brainstem Neurons During Mesencephalic Locomotor Region-Evoked Locomotion in the Cat

Descending Influences on Vestibulospinal and Vestibulosympathetic Reflexes

Integration of vestibular and hindlimb inputs by vestibular nucleus neurons: multisensory influences on postural control

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