Skip to main content
Top
Published in: Experimental Brain Research 8/2015

01-08-2015 | Research Article

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

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

Published in: Experimental Brain Research | Issue 8/2015

Login to get access

Abstract

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 suggests that they play different roles in coordinating postural responses during locomotion and other movements which entail changes in limb position.
Literature
go back to reference Asanuma C, Thach WT, Jones EG (1983) Brainstem and spinal projections of the deep cerebellar nuclei in the monkey, with observations on the brainstem projections of the dorsal column nuclei. Brain Res 286:299–322PubMedCrossRef Asanuma C, Thach WT, Jones EG (1983) Brainstem and spinal projections of the deep cerebellar nuclei in the monkey, with observations on the brainstem projections of the dorsal column nuclei. Brain Res 286:299–322PubMedCrossRef
go back to reference Berman AI (1968) The brain stem of the cat. University of Wisconsin Press, Madison Berman AI (1968) The brain stem of the cat. University of Wisconsin Press, Madison
go back to reference Bosco G, Poppele RE (1993) Broad directional tuning in spinal projections to the cerebellum. J Neurophysiol 70:863–866PubMed Bosco G, Poppele RE (1993) Broad directional tuning in spinal projections to the cerebellum. J Neurophysiol 70:863–866PubMed
go back to reference Bosco G, Poppele RE (2001) Proprioception from a spinocerebellar perspective. Physiol Rev 81:539–568PubMed Bosco G, Poppele RE (2001) Proprioception from a spinocerebellar perspective. Physiol Rev 81:539–568PubMed
go back to reference Catanzaro MF, Miller DJ, Cotter LA, McCall AA, Yates BJ (2014) Integration of vestibular and gastrointestinal inputs by cerebellar fastigial nucleus neurons: multisensory influences on motion sickness. Exp Brain Res 232:2581–2589. doi:10.1007/s00221-014-3898-9 PubMedCrossRef Catanzaro MF, Miller DJ, Cotter LA, McCall AA, Yates BJ (2014) Integration of vestibular and gastrointestinal inputs by cerebellar fastigial nucleus neurons: multisensory influences on motion sickness. Exp Brain Res 232:2581–2589. doi:10.​1007/​s00221-014-3898-9 PubMedCrossRef
go back to reference Eccles JC, Rantucci T, Sabah NH, Taborikova H (1974a) Somatotopic studies on cerebellar fastigial cells. Exp Brain Res 19:100–118PubMedCrossRef Eccles JC, Rantucci T, Sabah NH, Taborikova H (1974a) Somatotopic studies on cerebellar fastigial cells. Exp Brain Res 19:100–118PubMedCrossRef
go back to reference Eccles JC, Sabah NH, Taborikova H (1974b) Excitatory and inhibitory responses of neurones of the cerebellar fastigial nucleus. Exp Brain Res 19:61–77PubMedCrossRef Eccles JC, Sabah NH, Taborikova H (1974b) Excitatory and inhibitory responses of neurones of the cerebellar fastigial nucleus. Exp Brain Res 19:61–77PubMedCrossRef
go back to reference Fredrickson JM, Schwarz D, Kornhuber HH (1966) Convergence and interaction of vestibular and deep somatic afferents upon neurons in the vestibular nuclei of the cat. Acta Otolaryngol 61:168–188PubMedCrossRef Fredrickson JM, Schwarz D, Kornhuber HH (1966) Convergence and interaction of vestibular and deep somatic afferents upon neurons in the vestibular nuclei of the cat. Acta Otolaryngol 61:168–188PubMedCrossRef
go back to reference Ghelarducci B (1973) Responses of the cerebellar fastigial neurones to tilt. Pflugers Arch 344:195–206PubMedCrossRef Ghelarducci B (1973) Responses of the cerebellar fastigial neurones to tilt. Pflugers Arch 344:195–206PubMedCrossRef
go back to reference Ghelarducci B, Pompeiano O, Spyer KM (1974) Distribution of the neuronal responses to static tilts within the cerebellar fastigial nucleus. Arch Ital Biol 112:126–141PubMed Ghelarducci B, Pompeiano O, Spyer KM (1974) Distribution of the neuronal responses to static tilts within the cerebellar fastigial nucleus. Arch Ital Biol 112:126–141PubMed
go back to reference Gray C, Perciavalle V, Poppele R (1993) Sensory responses to passive hindlimb joint rotation in the cerebellar cortex of the cat. Brain Res 622:280–284PubMedCrossRef Gray C, Perciavalle V, Poppele R (1993) Sensory responses to passive hindlimb joint rotation in the cerebellar cortex of the cat. Brain Res 622:280–284PubMedCrossRef
go back to reference Homma Y, Nonaka S, Matsuyama K, Mori S (1995) Fastigiofugal projection to the brainstem nuclei in the cat: an anterograde PHA-L tracing study. Neurosci Res 23:89–102PubMedCrossRef Homma Y, Nonaka S, Matsuyama K, Mori S (1995) Fastigiofugal projection to the brainstem nuclei in the cat: an anterograde PHA-L tracing study. Neurosci Res 23:89–102PubMedCrossRef
go back to reference Huber J, Grottel K, Mrowczynski W, Krutki P (1999) Spinoreticular neurons in the second sacral segment of the feline spinal cord. Neurosci Res 34:59–65PubMedCrossRef Huber J, Grottel K, Mrowczynski W, Krutki P (1999) Spinoreticular neurons in the second sacral segment of the feline spinal cord. Neurosci Res 34:59–65PubMedCrossRef
go back to reference Ito M, Udo M, Mano N, Kawai N (1970) Synaptic action of the fastigiobulbar impulses upon neurones in the medullary reticular formation and vestibular nuclei. Exp Brain Res 11:29–47PubMedCrossRef Ito M, Udo M, Mano N, Kawai N (1970) Synaptic action of the fastigiobulbar impulses upon neurones in the medullary reticular formation and vestibular nuclei. Exp Brain Res 11:29–47PubMedCrossRef
go back to reference Marsden JF, Castellote J, Day BL (2002) Bipedal distribution of human vestibular-evoked postural responses during asymmetrical standing. J Physiol 542:323–331PubMedCentralPubMedCrossRef Marsden JF, Castellote J, Day BL (2002) Bipedal distribution of human vestibular-evoked postural responses during asymmetrical standing. J Physiol 542:323–331PubMedCentralPubMedCrossRef
go back to reference Matsushita M (1999) Projections from the lowest lumbar and sacral-caudal segments to the cerebellar nuclei in the rat, studied by anterograde axonal tracing. J Comp Neurol 404:21–32PubMedCrossRef Matsushita M (1999) Projections from the lowest lumbar and sacral-caudal segments to the cerebellar nuclei in the rat, studied by anterograde axonal tracing. J Comp Neurol 404:21–32PubMedCrossRef
go back to reference Maunz RA, Pitts NG, Peterson BW (1978) Cat spinoreticular neurons: locations, responses and changes in responses during repetitive stimulation. Brain Res 148:365–379PubMedCrossRef Maunz RA, Pitts NG, Peterson BW (1978) Cat spinoreticular neurons: locations, responses and changes in responses during repetitive stimulation. Brain Res 148:365–379PubMedCrossRef
go back to reference McKelvey-Briggs DK, Saint-Cyr JA, Spence SJ, Partlow GD (1989) A reinvestigation of the spinovestibular projection in the cat using axonal transport techniques. Anat Embryol 180:281–291PubMedCrossRef McKelvey-Briggs DK, Saint-Cyr JA, Spence SJ, Partlow GD (1989) A reinvestigation of the spinovestibular projection in the cat using axonal transport techniques. Anat Embryol 180:281–291PubMedCrossRef
go back to reference Osborn CE, Poppele RE (1992) Parallel distributed network characteristics of the DSCT. J Neurophysiol 68:1100–1112PubMed Osborn CE, Poppele RE (1992) Parallel distributed network characteristics of the DSCT. J Neurophysiol 68:1100–1112PubMed
go back to reference Oscarsson O (1965) Functional organization of the spino- and cuneocerebellar tracts. Physiol Rev 45:495–522PubMed Oscarsson O (1965) Functional organization of the spino- and cuneocerebellar tracts. Physiol Rev 45:495–522PubMed
go back to reference Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMed Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMed
go back to reference Schor RH, Angelaki DE (1992) The algebra of neural response vectors. Ann N Y Acad Sci 656:190–204PubMedCrossRef Schor RH, Angelaki DE (1992) The algebra of neural response vectors. Ann N Y Acad Sci 656:190–204PubMedCrossRef
go back to reference Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146PubMed Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146PubMed
go back to reference Siebold C, Glonti L, Glasauer S, Buttner U (1997) Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J Neurophysiol 77:1432–1446PubMed Siebold C, Glonti L, Glasauer S, Buttner U (1997) Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J Neurophysiol 77:1432–1446PubMed
go back to reference Stanojevic M (1981) Responses of cerebellar fastigial neurons to neck and macular vestibular inputs. Pflugers Arch 391:267–272PubMed Stanojevic M (1981) Responses of cerebellar fastigial neurons to neck and macular vestibular inputs. Pflugers Arch 391:267–272PubMed
go back to reference Stanojevic M, Erway L, Ghelarducci B, Pompeiano O, Willis WD Jr (1980) A comparison of the response characteristics of cerebellar fastigial and vermal cortex neurons to sinusoidal stimulation of macular vestibular receptors. Pflugers Arch 385:95–104PubMedCrossRef Stanojevic M, Erway L, Ghelarducci B, Pompeiano O, Willis WD Jr (1980) A comparison of the response characteristics of cerebellar fastigial and vermal cortex neurons to sinusoidal stimulation of macular vestibular receptors. Pflugers Arch 385:95–104PubMedCrossRef
go back to reference Welgampola MS, Colebatch JG (2001) Vestibulospinal reflexes: quantitative effects of sensory feedback and postural task. Exp Brain Res 139:345–353PubMedCrossRef Welgampola MS, Colebatch JG (2001) Vestibulospinal reflexes: quantitative effects of sensory feedback and postural task. Exp Brain Res 139:345–353PubMedCrossRef
go back to reference Wilson VJ, Kato M, Thomas RC, Peterson BW (1966) Excitation of lateral vestibular neurons by peripheral afferent fibers. J Neurophysiol 29:508–529PubMed Wilson VJ, Kato M, Thomas RC, Peterson BW (1966) Excitation of lateral vestibular neurons by peripheral afferent fibers. J Neurophysiol 29:508–529PubMed
go back to reference Wilson VJ, Uchino Y, Maunz RA, Susswein A, Fukushima K (1978) Properties and connections of cat fastigiospinal neurons. Exp Brain Res 32:1–17PubMedCrossRef Wilson VJ, Uchino Y, Maunz RA, Susswein A, Fukushima K (1978) Properties and connections of cat fastigiospinal neurons. Exp Brain Res 32:1–17PubMedCrossRef
Metadata
Title
Hindlimb movement modulates the activity of rostral fastigial nucleus neurons that process vestibular input
Authors
Andrew A. McCall
Daniel J. Miller
Michael F. Catanzaro
Lucy A. Cotter
Bill J. Yates
Publication date
01-08-2015
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 8/2015
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-015-4311-z

Other articles of this Issue 8/2015

Experimental Brain Research 8/2015 Go to the issue