Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats
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  • 作者:Chun-Hong Lai ; Chun-Wai Ma ; Suk-King Lai ; Lei Han…
  • 关键词:Development ; Fos expression ; Glutamate receptor ; Head rotation
  • 刊名:Brain Structure and Function
  • 出版年:2016
  • 出版时间:January 2016
  • 年:2016
  • 卷:221
  • 期:1
  • 页码:217-238
  • 全文大小:6,290 KB
  • 参考文献:Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247CrossRef PubMed
    Altman J, Bayer SA (1980) Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J Comp Neurol 194:877–904CrossRef PubMed
    Apps R (1990) Columnar organisation of the inferior olive projection to the posterior lobe of the rat cerebellum. J Comp Neurol 302:236–254CrossRef PubMed
    Azizi SA, Woodward DJ (1987) Inferior olivary nuclear complex of the rat: morphology and comments on the principles of organization within the olivocerebellar system. J Comp Neurol 263:467–484CrossRef PubMed
    Balaban CD, Beryozkin G (1994) Organization of vestibular nucleus projections to the caudal dorsal cap of kooy in rabbits. Neuroscience 62:1217–1236CrossRef PubMed
    Baloh RW, Halmagyi GM (1996) Disorders of the vestibular system. Oxford University Press, New York
    Barmack NH (1996) GABAergic pathways convey vestibular information to the beta nucleus and dorsomedial cell column of the inferior olive. Ann N Y Acad Sci 781:541–552CrossRef PubMed
    Blanks RH, Torigoe Y (1989) Orientation of the semicircular canals in rats. Brain Res 487:278–287CrossRef PubMed
    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 67:639–647PubMed
    Bruschini L, Andre P, Pompeiano O, Manzoni D (2006) Responses of Purkinje-cells of the cerebellar anterior vermis to stimulation of vestibular and somatosensory receptors. Neuroscience 142:235–245CrossRef PubMed
    Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brainstem lesions in monkey. J Neurophysiol 57:1383–1409PubMed
    Chan RK, Sawchenko PE (1994) Spatially and temporally differentiated patterns of c-fos expression in brain stem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J Comp Neurol 348:433–460CrossRef PubMed
    Chan YS, Hwang JC, Cheung YM (1979) Vestibular function of saccule in cats as indicated by the response of Deiters’ nucleus to static tilts. Exp Brain Res 35:591–594CrossRef PubMed
    Chan YS, Chen CW, Lai CH (1996) Response of medial medullary reticular neurons to otolith stimulation during bidirectional off-vertical axis rotation of the cat. Brain Res 732:159–168CrossRef PubMed
    Chen X, Herbert J (1995) Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64:675–685CrossRef PubMed
    Chen LW, Lai CH, Law HY, Yung KK, Chan YS (2003) Quantitative study of the coexpression of Fos and N-methyl-d aspartate (NMDA) receptor subunits in otolith-related vestibular nuclear neurons of rats. J Comp Neurol 460:292–301CrossRef PubMed
    Cheron G, Godaux E, Laune JM, Vanderkelen B (1988) Lesions in the cat prepositus complex: effects on the vestibulo-ocular reflex and saccades. J Physiol 372:75–94CrossRef
    Clements JD, Lester RA, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1498–1501CrossRef PubMed
    Cline HT, Constantine-Paton M (1989) NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3:413–426CrossRef PubMed
    Coggeshall RE, Lekan HA (1996) Methods for determining numbers of cells or synapses: a case for more uniform standards of review. J Comp Neurol 364:6–15CrossRef PubMed
    Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477–505CrossRef PubMed
    Curthoys IS (1979a) The development of function of horizontal semicircular canal primary neurons in the rat. Brain Res 167:41–52CrossRef PubMed
    Curthoys IS (1979b) The vestibulo-ocular reflex in newborn rats. Acta Otolaryngol 87:484–489CrossRef PubMed
    Curthoys IS (1982) Postnatal developmental changes in the response of rat primary horizontal semicircular canal neurons to sinusoidal angular accelerations. Exp Brain Res 47:295–300PubMed
    Curthoys IS, Curthoys EJ, Blanks RH, Markham CH (1975) The orientation of the semicircular canals in the guinea pig. Acta Otolaryngol 80:197–205CrossRef PubMed
    Curthoys IS, Betts GA, Burgess AM, MacDougall HG, Cartwright AD, Halmagyi GM (1999) The planes of the utricular and saccular maculae of the guinea pig. Ann N Y Acad Sci 871:27–34CrossRef PubMed
    Dampney RA, Horiuchi J (2003) Functional organisation of central cardiovascular pathways: studies using c-fos gene expression. Prog Neurobiol 71:359–384CrossRef PubMed
    De Zeeuw CI, Wentzel P, Mugnaini E (1993) Fine structure of the dorsal cap of the inferior olive and its GABAergic and non-GABAergic input from the nucleus prepositus hypoglossi in rat and rabbit. J Comp Neurol 327:63–82CrossRef PubMed
    De Zeeuw CI, Gerrits NM, Voogd J, Leonard CS, Simpson JI (1994) The rostral dorsal cap and ventrolateral outgrowth of the rabbit inferior olive receive a GABAergic input from dorsal group Y and the ventral dentate nucleus. J Comp Neurol 341:420–432CrossRef PubMed
    De Zeeuw CI, Simpson JI, Hooenraad CC, Galijart N, Koekkoek SK, Ruigrok TJ (1998) Microcircuitry and function of the inferior olive. Trends Neurosci 21:391–400CrossRef PubMed
    Dechesne C, Mbiene JP, Sans A (1986) Postnatal development of vestibular receptor surfaces in the rat. Acta Otolaryngol 101:11–18CrossRef PubMed
    Dutia MB, Johnston AR (1998) Development of action potentials and apamin-sensitive after-potentials in mouse vestibular nucleus neurones. Exp Brain Res 118:148–154CrossRef PubMed
    Eugène D, Idoux E, Beraneck M, Moore LE, Vidal PP (2011) Intrinsic membrane properties of central vestibular neurons in rodents. Exp Brain Res 210:423–436CrossRef PubMed
    Fagerson MH, Barmack NH (1995) Responses to vertical vestibular stimulation of neurons in the nucleus reticularis gigantocellularis in rabbits. J Neurophysiol 73:2378–2391PubMed
    Faulstich BM, Onori KA, du Lac S (2004) Comparison of plasticity and development of mouse optokinetic and vestibulo-ocular reflexes suggests differential gain control mechanisms. Vision Res 44:3419–3427CrossRef PubMed
    Fernández C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970–984PubMed
    Fukushima K, Chin S, Fukushima J, Tanaka M (1996) Simple-spike activity of floccular Purkinje cells responding to sinusoidal vertical rotation and optokinetic stimuli in alert cats. Neurosci Res 24:275–289CrossRef PubMed
    Fushiki H, Barmack NH (1997) Topography and reciprocal activity of cerebellar Purkinje cells in the uvula-nodulus modulated by vestibular stimulation. J Neurophysiol 78:3083–3094PubMed
    Gaytan SP, Pasaro R (2012) Neonatal caffeine treatment up-regulates adenosine receptors in brainstem and hypothalamic cardio-respiratory related nuclei of rat pups. Exp Neurol 237:247–259CrossRef PubMed
    Gerrits NM, Voogd J, Magras IN (1985) Vestibular afferents of the inferior olive and the vestibulo-olivo-cerebellar climbing fiber pathway to the flocculus in the cat. Brain Res 332:325–336CrossRef PubMed
    Hard E, Larsson K (1975) Development of air righting in rats. Brain Behav Evol 11:53–59CrossRef PubMed
    Hess BJ, Dieringer N (1991) Spatial organization of linear vestibuloocular reflexes of the rat: responses during horizontal and vertical linear acceleration. J Neurophysiol 66:1805–1818PubMed
    Holstein GR, Martinelli GP, Cohen B (1999) The ultrastructure of GABA-immunoreactive vestibular commissural neurons related to velocity storage in the monkey. Neuroscience 93:171–181CrossRef PubMed
    Janusonis S, Fite K (2001) Diurnal variation of c-fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 440:31–42CrossRef PubMed
    Kakizawa S, Miyazaki T, Yanagihara D, Iino M, Watanabe M, Kano M (2005) Maintenance of presynaptic function by AMPA receptor-mediated excitatory postsynaptic activity in adult brain. Proc Natl Acad Sci USA 102:19180–19185PubMedCentral CrossRef PubMed
    Kasper J, Schor RH, Wilson VJ (1988) Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation. J Neurophysiol 60:1753–1764PubMed
    Kaufman GD, Anderson JH, Beitz AJ (1992) Fos-defined activity in rat brainstem following centripetal acceleration. J Neurosci 12:4489–4500PubMed
    Kaufman GD, Anderson JH, Beitz AJ (1993) Otolith
    ain stem connectivity: evidence for differential neural activation by vestibular hair cells based on quantification of FOS expression in unilateral labyrinthectomized rats. J Neurophysiol 70:117–127PubMed
    Kinney GA, Peterson BW, Slater NT (1994) The synaptic activation of N-methyl-d -aspartate receptors in the rat medial vestibular nucleus. J Neurophysiol 72:1588–1595PubMed
    Lai CH, Chan YS (2001) Spontaneous discharge and response characteristics of central otolith neurons of rats during postnatal development. Neuroscience 103:275–288CrossRef PubMed
    Lai CH, Tse YC, Shum DK, Yung KK, Chan YS (2004) Fos expression in otolith-related brainstem neurons of postnatal rats following off-vertical axis rotation. J Comp Neurol 470:282–296CrossRef PubMed
    Lai SK, Lai CH, Yung KK, Shum DK, Chan YS (2006) Maturation of otolith-related brainstem neurons in the detection of vertical linear acceleration in rats. Eur J Neurosci 23:2341–2346CrossRef
    Lai SK, Lai CH, Tse YC, Yung KK, Shum DK, Chan YS (2008) Developmental maturation of ionotropic glutamate receptor subunits in rat vestibular nuclear neurons responsive to vertical linear acceleration. Eur J Neurosci 28:2157–2172CrossRef PubMed
    Lai CH, Yiu CN, Lai SK, Ng KP, Shum DK, Chan YS (2010) Maturation of canal-related brainstem neurons in the detection of horizontal angular acceleration in rats. J Comp Neurol 518:1742–1763CrossRef PubMed
    Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser MB (2010) Development of the spatial representation system in the rat. Science 328:1576–1580CrossRef PubMed
    Lannou J, Precht W, Cazin L (1979) The postnatal development of functional properties of central vestibular neurons in the rat. Brain Res 7:219–232CrossRef
    Lannou J, Precht W, Cazin L (1980) Development of optokinetic responses in vestibular nuclear neurons in the young rat. Brain Res 202:217–222CrossRef PubMed
    Laouris Y, Kalli-Laouri J, Schwartze P (1990) The postnatal development of the air-righting reaction in albino rats. Quantitative analysis of normal development and the effect of preventing neck-torso-pelvis rotations. Behav Brain Res 37:37–44CrossRef PubMed
    Li C, Han L, Ma CW, Lai SK, Lai CH, Shum DK, Chan YS (2013) Maturation profile of inferior olivary neurons expressing ionotropic glutamate receptors in rats: role in coding linear accelerations. Brain Struct Funct 218:833–850PubMedCentral CrossRef PubMed
    Ma CW, Lai CH, Lai SK, Tse YC, Yung KK, Shum DK, Chan YS (2010) Developmental distribution of vestibular nuclear neurons responsive to different speeds of horizontal translation. Brain Res 1326:62–67CrossRef PubMed
    Macdougall HG, McGarvie LA, Halmagyi GM, Curthoys IS, Weber KP (2013) The video Head Impulse Test (vHIT) detects vertical semicircular canal dysfunction. PLoS ONE 8:e61488PubMedCentral CrossRef PubMed
    Mariani J, Changeux JP (1981) Ontogenesis of olivocerebellar relationships. II. Spontaneous activity of inferior olivary neurons and climbing fiber mediated activity of cerebellar Purkinje cells in developing rats. J Neurosci 1:703–709PubMed
    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
    Moratalla R, Elibol B, Vallejo M, Graybiel AM (1996) Network-level changes in expression of inducible Fos-Jun proteins in the striatum during chronic cocaine treatment and withdrawal. Neuron 17:147–156CrossRef PubMed
    Morgan JI, Curran T (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421–451CrossRef PubMed
    Mori RL, Bergsman AE, Holmes MJ, Yates BJ (2001) Role of the medial medullary reticular formation in relaying vestibular signals to the diaphragm and abdominal muscles. Brain Res 902:82–91CrossRef PubMed
    Morris RJ, Beech JN, Heizmann CW (1988) Two distinct phases and mechanisms of axonal growth shown by primary vestibular fibres in the brain, demonstrated by parvalbumin immunohistochemistry. Neuroscience 27:571–596CrossRef PubMed
    Moy JD, Miller DJ, Catanzaro MF, Boyle BM, Ogburn SW, Cotter LA, Yates BJ, McCall AA (2012) Responses of neurons in the caudal medullary lateral tegmental field to visceral inputs and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 303:R929–R940PubMedCentral CrossRef PubMed
    Muir GM, Brown JE, Carey JP, Hirvonen TP, Della Santina CC, Minor LB, Taube JS (2009) Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J Neurosci 29:14521–14533PubMedCentral CrossRef PubMed
    Murphy GJ, du Lac S (2001) Postnatal development of spike generation in rat medial vestibular nucleus neurons. J Neurophysiol 85:1899–1906PubMed
    Parrad J, Cottereau P (1977) Appearance of rotary reactions in the newborn rat. Physiol Behav 18:1017–1020CrossRef PubMed
    Paxino G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, San Diego
    Paxinos G, Ashwell KWS, Tork I (1994) Atlas of the developing rat nervous system. Academic Press, San Diego
    Peterson BW (2004) Current approaches and future directions to understanding control of head movement. Prog Brain Res 143:369–381PubMed
    Peterson BW, Fukushima K, Hirai N, Schor RH, Wilson VJ (1980) Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J Neurophysiol 43:1236–1250PubMed
    Reisinger E, Meintrup D, Oliver D, Fakler B (2010) Gene expression associated with the onset of hearing detected by differential display in rat organ of Corti. Eur J Hum Genet 18:1327–1332PubMedCentral CrossRef PubMed
    Rinaman L, Stricker EM, Hoffman GE, Verbalis JG (1997) Central c-Fos expression in neonatal and adult rats after subcutaneous injection of hypertonic saline. Neuroscience 79:1165–1175CrossRef PubMed
    Ruigrok TJ (2003) Collateralization of climbing and mossy fibers projecting to the nodulus and flocculus of the rat cerebellum. J Comp Neurol 466:278–298CrossRef PubMed
    Saper CB (1996) Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol 364:365
    Schnupp JW, King AJ, Smith AL, Thompson ID (1995) NMDA-receptor antagonists disrupt the formation of the auditory space map in the mammalian superior colliculus. J Neurosci 15:1516–1531PubMed
    Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492PubMed
    Shu SY, Ju G, Fan LZ (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85:169–171CrossRef PubMed
    Simon DK, Prusky GT, O’Leary DD, Constantine-Paton M (1992) N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc Natl Acad Sci USA 89:10593–10597PubMedCentral CrossRef PubMed
    Smith AL, Cordery PM, Thompson ID (1995) Manufacture and release characteristics of Elvax polymers containing glutamate receptor antagonists. J Neurosci Methods 60:211–217CrossRef PubMed
    Sugihara I, Wu HS, Shinoda Y (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci 21:7715–7723PubMed
    Takada SH, Sampaio CA, Allemandi W, Ito PH, Takase LF, Nogueira MI (2011) A modified rat model of neonatal anoxia: Development and evaluation by pulseoximetry, arterial gasometry and Fos immunoreactivity. J Neurosci Methods 198:62–69CrossRef PubMed
    Tomko DL, Peterka RJ, Schor RH (1981) Responses to head tilt in cat eighth nerve afferents. Exp Brain Res 41:216–221PubMed
    Tse YC, Lai CH, Lai SK, Liu JX, Yung KK, Shum DK, Chan YS (2008) Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity-related horizontal orientations. J Comp Neurol 508:343–364CrossRef PubMed
    Wallace H, Glazewski S, Liming K, Fox K (2001) The role of cortical activity in experience-dependent potentiation and depression of sensory responses in rat barrel cortex. J Neurosci 21:3881–3894PubMed
    Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–1576PubMedCentral CrossRef PubMed
    Wilson VJ, Schor RH (1999) The neural substrate of the vestibulocollic reflex. What needs to be learned. Exp Brain Res 129:483–493CrossRef PubMed
    Wong HM, Yeung KW, Lam KO, Tam V, Chu PK, Luk KD, Cheung KM (2010) A biodegradable polymer-based coating to control the performance of magnesium alloy orthopaedic implants. Biomaterials 31:2084–2096CrossRef PubMed
    Wong HM, Wu S, Chu PK, Cheng SH, Luk KD, Cheung KM, Yeung KW (2013) Low-modulus Mg/PCL hybrid bone substitute for osteoporotic fracture fixation. Biomaterials 34:7016–7032CrossRef PubMed
    Wubbels RJ, Sondag HN, van Marle J, de Jong HA (2002) Effects of hypergravity on the morphological properties of the vestibular sensory epithelium. I. Long-term exposure of rats after full maturation of the labyrinths. Brain Res Bull 57:677–682CrossRef PubMed
    Yakhnitsa V, Barmack NH (2006) Antiphasic Purkinje cell responses in mouse uvula-nodulus are sensitive to static roll-tilt and topographically organized. Neuroscience 143:615–626CrossRef PubMed
    Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, Angelaki DE (2007) Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54:973–985CrossRef PubMed
    Yates BJ, Jian BJ, Cotter LA, Cass SP (2000) Responses of vestibular nucleus neurons to tilt following chronic bilateral removal of vestibular inputs. Exp Brain Res 130:151–158CrossRef PubMed
    Yoder RM, Taube JS (2009) Head direction cell activity in mice: robust directional signal depends on intact otolith organs. J Neurosci 29:1061–1076PubMedCentral CrossRef PubMed
  • 作者单位:Chun-Hong Lai (1)
    Chun-Wai Ma (1) (2)
    Suk-King Lai (1) (4) (5)
    Lei Han (1) (4)
    Hoi-Man Wong (3)
    Kelvin Wai-Kwok Yeung (3)
    Daisy Kwok-Yan Shum (2) (4)
    Ying-Shing Chan (1) (4)

    1. Department of Physiology, LKS Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Hong Kong, People’s Republic of China
    2. Department of Biochemistry, LKS Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Hong Kong, People’s Republic of China
    4. Research Centre of Heart, Brain, Hormone and Healthy Aging, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, People’s Republic of China
    5. Department of Neurophysiology, Tokyo University, Tokyo, 113-0033, Japan
    3. Department of Orthopaedics and Traumatology, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong, People’s Republic of China
  • 刊物主题:Neurosciences; Cell Biology; Neurology;
  • 出版者:Springer Berlin Heidelberg
  • ISSN:1863-2661
文摘
The recognition of head orientation in the adult involves multi-level integration of inputs within the central vestibular circuitry. How the different inputs are recruited during postnatal development remains unclear. We hypothesize that glutamatergic transmission at the vestibular nucleus contributes to developmental registration of head orientations along the vestibulo-olivary pathway. To investigate the maturation profile by which head rotational signals are registered in the brainstem, we used sinusoidal rotations on the orthogonal planes of the three pairs of semicircular canals. Fos expression was used as readout of neurons responsive to the rotational stimulus. Neurons in the vestibular nucleus and prepositus hypoglossal nucleus responded to all rotations as early as P4 and reached adult numbers by P21. In the reticular formation and inferior olive, neurons also responded to horizontal rotations as early as P4 but to vertical rotations not until P21 and P25, respectively. Neuronal subpopulations that distinguish between rotations activating the orthogonally oriented vertical canals were identifiable in the medial and spinal vestibular nuclei by P14 and in the inferior olivary subnuclei IOβ and IOK by P25. Neonatal perturbation of glutamate transmission in the vestibular nucleus was sufficient to derange formation of this distribution in the inferior olive. This is the first demonstration that developmental refinement of glutamatergic synapses in the central vestibular circuitry is essential for developmental registration of head rotational signals in the brainstem. Keywords Development Fos expression Glutamate receptor Head rotation

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