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

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Abstract

The integration of inputs from vestibular and proprioceptive sensors within the central nervous system is critical to postural regulation. We recently demonstrated in both decerebrate and conscious cats that labyrinthine and hindlimb inputs converge onto vestibular nucleus neurons. The pontomedullary reticular formation (pmRF) also plays a key role in postural control, and additionally participates in regulating locomotion. Thus, we hypothesized that like vestibular nucleus neurons, pmRF neurons integrate inputs from the limb and labyrinth. To test this hypothesis, we recorded the responses of pmRF neurons to passive ramp-and-hold movements of the hindlimb and to whole-body tilts, in both decerebrate and conscious felines. We found that pmRF neuronal activity was modulated by hindlimb movement in the rostral-caudal plane. Most neurons in both decerebrate (83% of units) and conscious (61% of units) animals encoded both flexion and extension movements of the hindlimb. In addition, hindlimb somatosensory inputs converged with vestibular inputs onto pmRF neurons in both preparations. Pontomedullary reticular formation neurons receiving convergent vestibular and limb inputs likely participate in balance control by governing reticulospinal outflow.

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References

  • Abzug C, Peterson BW (1973) Antidromic stimulation in the ponto-medullary reticular formation of local axon branches of contralateral vestibular neurons. Brain Res 64:407–413

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Arshian MS, Hobson CE, Catanzaro MF et al (2014) Vestibular nucleus neurons respond to hindlimb movement in the decerebrate cat. J Neurophysiol 111:2423–2432. doi:10.1152/jn.00855.2013

    Article  PubMed  PubMed Central  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  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868

    CAS  PubMed  Google Scholar 

  • Carleton SC, Carpenter MB (1983) Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res 278:29–51

    Article  CAS  PubMed  Google Scholar 

  • Drew T, Dubuc R, Rossignol S (1986) Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. J Neurophysiol 55:375–401

    CAS  PubMed  Google Scholar 

  • Drew T, Cabana T, Rossignol S (1996) Responses of medullary reticulospinal neurones to stimulation of cutaneous limb nerves during locomotion in intact cats. Exp Brain Res 111:153–168

    Article  CAS  PubMed  Google Scholar 

  • Eccles JC, Nicoll RA, Schwarz WF, Taborikova H, Willey TJ (1975) Reticulospinal neurons with and without monosynaptic inputs from cerebellar nuclei. J Neurophysiol 38:513–530

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Grasso C, Barresi M, Scattina E, Orsini P, Vignali E, Bruschini L, Manzoni D (2011) Tuning of human vestibulospinal reflexes by leg rotation. Hum Mov Sci 30:296–313. doi:10.1016/j.humov.2010.07.018

    Article  CAS  PubMed  Google Scholar 

  • Grillner S, Hongo T, Lund S (1971) Convergent effects on alpha motoneurones from the vestibulospinal tract and a pathway descending in the medial longitudinal fasciculus. Exp Brain Res 12:457–479

    Article  CAS  PubMed  Google Scholar 

  • Horak FB (2006) Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35(Suppl 2):ii7–ii11. doi:10.1093/ageing/afl077

    PubMed  Google Scholar 

  • Jian BJ, Shintani T, Emanuel BA, Yates BJ (2002) Convergence of limb, visceral, and vertical semicircular canal or otolith inputs onto vestibular nucleus neurons. Exp Brain Res 144:247–257. doi:10.1007/s00221-002-1042-8

    Article  CAS  PubMed  Google Scholar 

  • Kably B, Drew T (1998) Corticoreticular pathways in the cat. II. Discharge activity of neurons in area 4 during voluntary gait modifications. J Neurophysiol 80:406–424

    CAS  PubMed  Google Scholar 

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

  • Kasper J, Schor RH, Wilson VJ (1988b) Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction. J Neurophysiol 60:1765–1778

  • Keizer K, Kuypers HG (1984) Distribution of corticospinal neurons with collaterals to lower brain stem reticular formation in cat. Exp Brain Res 54:107–120

    Article  CAS  PubMed  Google Scholar 

  • Kennedy PM, Inglis JT (2002) Interaction effects of galvanic vestibular stimulation and head position on the soleus H reflex in humans. Clin Neurophysiol 113:1709–1714

    Article  PubMed  Google Scholar 

  • Kennedy PM, Cresswell AG, Chua R, Inglis JT (2004) Vestibulospinal influences on lower limb motoneurons. Can J Physiol Pharmacol 82:675–681. doi:10.1139/y04-080

    Article  CAS  PubMed  Google Scholar 

  • Ladpli R, Brodal A (1968) Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. Brain Res 8:65–96

    Article  CAS  PubMed  Google Scholar 

  • Manzoni D, Pompeiano O, Stampacchia G, Srivastava UC (1983) Responses of medullary reticulospinal neurons to sinusoidal stimulation of labyrinth receptors in decerebrate cat. J Neurophysiol 50:1059–1079

    CAS  PubMed  Google Scholar 

  • Marsden JF, Castellote J, Day BL (2002) Bipedal distribution of human vestibular-evoked postural responses during asymmetrical standing. J Physiol 542:323–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuyama K, Drew T (2000) Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. II. Walking on an inclined plane. J Neurophysiol 84:2257–2276

    CAS  PubMed  Google Scholar 

  • Maunz RA, Pitts NG, Peterson BW (1978) Cat spinoreticular neurons: locations, responses and changes in responses during repetitive stimulation. Brain Res 148:365–379

    Article  CAS  PubMed  Google Scholar 

  • McCall AA, Moy JD, DeMayo WM, Puterbaugh SR, Miller DJ, Catanzaro MF, Yates BJ (2013) 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. doi:10.1007/s00221-012-3376-1

    Article  PubMed  Google Scholar 

  • McCall AA, Miller DJ, Catanzaro MF, Cotter LA, Yates BJ (2015) Hindlimb movement modulates the activity of rostral fastigial nucleus neurons that process vestibular input. Exp Brain Res 233:2411–2419. doi:10.1007/s00221-015-4311-z

    Article  PubMed  PubMed Central  Google Scholar 

  • McCall AA, Miller DM, DeMayo WM, Bourdages GH, Yates BJ (2016) Vestibular nucleus neurons respond to hindlimb movement in the conscious cat. J Neurophysiol. doi:10.1152/jn.00414.2016

    PubMed  Google Scholar 

  • McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416–428

    CAS  PubMed  Google Scholar 

  • Miller DM, Cotter LA, Gandhi NJ et al (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. doi:10.1007/s00221-008-1359-z

  • Miller DM, Cotter LA, Gandhi NJ et al (2008b) Responses of rostral fastigial nucleus neurons of conscious cats to rotations in vertical planes. Neuroscience 155:317–325. doi:10.1016/j.neuroscience.2008.04.042

  • Orlovsky GN (1970) Connections of the reticulospinal neurons with the locomotor regions of the brainstem. Biophysics 15:178–186

    Google Scholar 

  • Perreault MC, Drew T, Rossignol S (1993) Activity of medullary reticulospinal neurons during fictive locomotion. J Neurophysiol 69:2232–2247

    CAS  PubMed  Google Scholar 

  • Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118

    CAS  PubMed  Google Scholar 

  • Peterson BW, Abzug C (1975) Properties of projections from vestibular nuclei to medial reticular formation in the cat. J Neurophysiol 38:1421–1435

    CAS  PubMed  Google Scholar 

  • Peterson BW, Anderson ME, Filion M (1974) Responses of ponto-medullary reticular neurons to cortical, tectal and cutaneous stimuli. Exp Brain Res 21:19–44

    Article  CAS  PubMed  Google Scholar 

  • Peterson BW, Franck JI, Daunton NG (1976) Changes in responses of medial pontomedullary reticular neurons during repetitive cutaneous, vestibular, cortical, and tectal stimulation. J Neurophysiol 39:564–581

    CAS  PubMed  Google Scholar 

  • Pompeiano O, Manzoni D, Srivastava UC, Stampacchia G (1984) Convergence and interaction of neck and macular vestibular inputs on reticulospinal neurons. Neuroscience 12:111–128

    Article  CAS  PubMed  Google Scholar 

  • Prentice SD, Drew T (2001) Contributions of the reticulospinal system to the postural adjustments occurring during voluntary gait modifications. J Neurophysiol 85:679–698

    CAS  PubMed  Google Scholar 

  • Schepens B, Drew T (2003) Strategies for the integration of posture and movement during reaching in the cat. J Neurophysiol 90:3066–3086. doi:10.1152/jn.00339.2003

    Article  PubMed  Google Scholar 

  • Schepens B, Drew T (2004) Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. J Neurophysiol 92:2217–2238. doi:10.1152/jn.01189.2003

    Article  PubMed  Google Scholar 

  • Schepens B, Stapley P, Drew T (2008) Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. J Neurophysiol 100:2235–2253. doi:10.1152/jn.01381.2007

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Segundo JP, Takenaka T, Encabo H (1967) Somatic sensory properties of bulbar reticular neurons. J Neurophysiol 30:1221–1238

    CAS  PubMed  Google Scholar 

  • Shefchyk SJ, Jordan LM (1985) Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region. J Neurophysiol 54:1101–1108

    CAS  PubMed  Google Scholar 

  • Siegel JM, Tomaszewski KS (1983) Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movements. J Neurophysiol 50:696–716

    CAS  PubMed  Google Scholar 

  • Stapley PJ, Drew T (2009) The pontomedullary reticular formation contributes to the compensatory postural responses observed following removal of the support surface in the standing cat. J Neurophysiol 101:1334–1350. doi:10.1152/jn.91013.2008

    Article  PubMed  Google Scholar 

  • Steeves JD, Jordan LM (1980) Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion. Neurosci Lett 20:283–288

    Article  CAS  PubMed  Google Scholar 

  • Tokita T, Ito Y, Takagi K (1989) Modulation by head and trunk positions of the vestibulo-spinal reflexes evoked by galvanic stimulation of the labyrinth. Observations by labyrinthine evoked EMG. Acta Otolaryngol 107:327–332

    Article  CAS  PubMed  Google Scholar 

  • Tokita T, Miyata H, Takagi K, Ito Y (1991) Studies on vestibulo-spinal reflexes by examination of labyrinthine-evoked EMGs of lower limbs. Acta Otolaryngol Suppl 481:328–332

    Article  CAS  PubMed  Google Scholar 

  • Welgampola MS, Colebatch JG (2001) Vestibulospinal reflexes: quantitative effects of sensory feedback and postural task. Exp Brain Res 139:345–353

    Article  CAS  PubMed  Google Scholar 

  • Wilson VJ (1991) Vestibulospinal and neck reflexes: interaction in the vestibular nuclei. Arch Ital Biol 129:43–52

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Melvill Jones G (1979) Mammalian Vestibular Physiology. Plenum Press, New York

    Book  Google Scholar 

  • Wilson VJ, Yoshida M (1969) Comparison of effects of stimulation of Deiters’ nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. J Neurophysiol 32:743–758

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Kato M, Thomas RC, Peterson BW (1966) Excitation of lateral vestibular neurons by peripheral afferent fibers. J Neurophysiol 29:508–529

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Lucy Cotter for providing technical assistance. This work was supported by the following grants from the NIH: T32-DC011499 (Derek Miller); F32-DC015157 (Derek Miller); T32-DC000066 (William DeMayo); and K08-DC013571 (Andrew McCall).

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Authors and Affiliations

  1. Department of Otolaryngology, Eye and Ear Institute, University of Pittsburgh, 203 Lothrop Street, Suite 500, Pittsburgh, PA, 15213, USA

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

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

    Bill J. Yates

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  1. Derek M. Miller
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  2. William M. DeMayo
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  3. George H. Bourdages
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  5. Bill J. Yates
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  6. Andrew A. McCall
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Correspondence to Andrew A. McCall.

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Miller, D.M., DeMayo, W.M., Bourdages, G.H. et al. Neurons in the pontomedullary reticular formation receive converging inputs from the hindlimb and labyrinth. Exp Brain Res 235, 1195–1207 (2017). https://doi.org/10.1007/s00221-017-4875-x

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  • DOI: https://doi.org/10.1007/s00221-017-4875-x

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