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Injections of β-noradrenergic substances in the flocculus of rabbits affect adaptation of the VOR gain

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Noradrenaline (NA) has been implicated as a neuromodulator in plasticity, presumably facilitating adaptive processes. Recent experiments by others have suggested a modulatory role of NA in adaptive changes in the vestibulo-ocular reflex (VOR). These experiments showed that general depletion of brain NA resulted in a decreased ability to produce adaptive changes in the VOR gain. In order to identify the specific brain region responsible for these effects, as well as the nature of the adrenoceptors involved, we injectedβ-adrenergic substances bilaterally into the flocculus of rabbits. The flocculus is known to receive noradrenergic afferents and, moreover, ablation of the flocculus interferes strongly with the normal adaptive changes in the VOR gain. We injected theβ-agonist isoproterenol and theβ-antagonist sotalol, and compared the adaptive capacity of the rabbits after these injections to that in a situation without injection. The rabbit was oscillated in a direction opposite to the direction of motion of the platform on which the rabbit was mounted, a condition which normally results in an increase in the VOR gain, measured either in light or in darkness. Injection of theβ-agonist did not greatly affect the adaptation of the VOR measured in the light. In darkness, the increase in gain after the injection of isoproterenol was larger than in the non-injection experiments in 9 out of 10 rabbits. Theβ-antagonist sotalol reduced the adaptation of the VOR gain significantly in the light, as well as in darkness. In a control condition without pressure for adaptation (only intermittent testing of the VOR gain over a period of 2.5 h), the gain of the VOR either remained unaffected or was only slightly affected by similar injections ofβ-adrenergic agents in individual rabbits. For the group as a whole, these effects were insignificant. We conclude from these results that noradrenergic systems facilitate the adaptation of the VOR gain to retinal slip in rabbits, without affecting the VOR gain directly. At least part of this influence is exerted throughβ-receptors located in the cerebellar flocculus.

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References

  • Abercrombie ED, Jacobs BL (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressfull and nonstressfull stimuli. J Neurosci 7:2837–2843

    Google Scholar 

  • Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61

    Google Scholar 

  • Berthoz A, Melvill Jones G (1985) Adaptive mechanisms in gaze control: facts and theories. Reviews of oculomotor research, Vol 1. Elsevier, Amsterdam

    Google Scholar 

  • Bloom FE, Hoffer BJ, Siggins GR (1971) Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. I. Localization of the fibers and their synapses. Brain Res 25:501–521

    Google Scholar 

  • Bylund DB, U'Prichard DC (1983) Characterization of α1 and α2-adrenergic receptors. Int Rev Neurobiol 24:343–431

    Google Scholar 

  • Collewijn H (1977) Eye- and head movements in freely moving rabbits. J Physiol (Lond) 266:471–498

    Google Scholar 

  • Collewijn H, Grootendorst AF (1978) Adaptation of the rabbit's vestibulo-ocular reflex to modified visual input: importance of stimulus conditions. Arch Ital Biol 116:273–280

    Google Scholar 

  • Collewijn H, Grootendorst AF (1979) Adaptation of optokinetic and vestibulo-ocular reflexes to modified visual input in the rabbit. In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Elsevier, Amsterdam, pp 771–781

    Google Scholar 

  • Collewijn H, Van der Steen J (1987) Visual control of the vestibulo-ocular reflex in the rabbit: a multi-level interaction. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. NATO ASI Series A, Vol 148. Plenum, Press, New York, pp 277–291

    Google Scholar 

  • d'Ascanio P, Bettini E, Pompeiano O (1985) Tonic inhibitory influences of locus coeruleus on the response gain of limb extensors to sinusoidal labyrinth and neck stimulations. Arch Ital Biol 123:69–100

    Google Scholar 

  • d'Ascanio P, Bettini E, Pompeiano O (1989) Inhibition of vestibulospinal reflexes during the episodes of postural atonia induced by unilateral lesion of the locus coeruleus in the decerebrate cat. Arch Ital Biol 127:81–97

    Google Scholar 

  • Dietrichs E (1988) Cerebellar cortical and nuclear afferents from the feline locus coeruleus complex. Neuroscience 27:77–92

    Google Scholar 

  • Edwards SB, Hendrickson A (1981) Neuroanatomical tracttracing methods. Plenum Press, New York

    Google Scholar 

  • Foote SL, Bloom FE, Aston-Jones G (1983) Nucleus locus coeruleus: new evidence of anatomical and physiological specificity. Physiol Rev 63:844–914

    Google Scholar 

  • Fuxe K (1965) Evidence for the existence of monoamine neurons in the central nervous system. IV. The distribution of monoamine terminals in the central nervous system. Acta Physiol Scand [Suppl] 247:37–85

    Google Scholar 

  • Gilbert P (1975) How the cerebellum could memorise movements. Nature 254:688–689

    Google Scholar 

  • Gordon B, Moran J, Trombley P, Soyke J (1986) Visual behaviour of monocularly deprived kittens treated with 6-hydroxydopamine. Brain Res 389:21–29

    Google Scholar 

  • Graf W, Simpson JI, Leonard CS (1988) The spatial organization of visual messages to the flocculus of the rabbit's cerebellum. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol 60:2091–2121

    Google Scholar 

  • Greenshaw AJ (1985) Electrical and chemical stimulation of brain tissue in vivo. In: Boulton AA, Baker GB (eds) General pneurochemical techniques: neuromethods (1). Humana Press, Cliton, pp 233–277

    Google Scholar 

  • Ito M (1984) The cerebellum and neural control. Raven Press, New York.

    Google Scholar 

  • Ito M, Shiida T, Yagi N, Yamamoto M (1974a) The cerebellar modification of rabbit's horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation. Proc Jpn Acad 50:85–89

    Google Scholar 

  • Ito M, Shiida T, Yagi N, Yamamoto M (1974b) Visual influence on rabbit horizontal vestibulo-ocular reflex presumably effected via the cerebellar flocculus. Brain Res 65:170–174

    Google Scholar 

  • Ito M, Jastreboff PJ, Miyashita Y (1979) Adaptive modification of the rabbit's horizontal vestibulo-ocular reflex during sustained vestibular and optokinetic stimulation. Exp Brain Res 37:17–30

    Google Scholar 

  • Ito M, Jastreboff PJ, Miyashita Y (1982) Specific effects of unilateral lesions in the flocculus upon eye movements in albino rabbits. Exp Brain Res 45:233–242

    Google Scholar 

  • Kasamatsu T (1987) Norepinephrine hypothesis for visual cortical plasticity: thesis, antithesis, and recent development. Curr Top Dev Biol 21:367–389

    Google Scholar 

  • Kasamatsu T, Pettigrew DJ (1976) Depletion of brain catecholamines: failure of ocular dominance shift after monocular occlusion in kittens. Science 194:202–209

    Google Scholar 

  • Kasamatsu T, Pettigrew JD, Ary M (1979) Restoration of visual cortical plasticity by local microperfusion of norepinephrine J Comp Neurol 185:163–182

    Google Scholar 

  • Kebabian JW, Zatz M, Romero JA, Axelrod J (1975) Rapid changes in rat pinealβ-adrenergic receptor: alteration in 1-[3H] alprenolol binding and adenylate cyclase. Proc Natl Acad Sci USA 72:3735–3739

    Google Scholar 

  • Keller EL, Smith MJ (1983) Suppressed visual adaptation of the vestibulo-ocular reflex in catecholamine depleted cats. Brain Res 258:323–327

    Google Scholar 

  • Kimoto Y, Satoh K, Sakumoto T, Tohyama M, Shimizu N (1978) Afferent fiber connections from the lower brain stem to the rat cerebellum by the horseradish peroxidase method combined with MAO staining, with special reference to noradrenergic neurons. J Hirnforsch 19:85–100

    Google Scholar 

  • Kimoto Y, Tohyama M, Satoh K, Sakumoto T, Takahashi Y, Shimizu N (1981) Fine structure of rat cerebellar noradrenaline terminals as visualized by potassium permanganate ‘in situ’: perfusion, fixation and method. Neuroscience 6:47–58

    Google Scholar 

  • Langer T, Fuchs AF, Scudder CA, Chubb MC (1985) Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 235:1–25

    Google Scholar 

  • Lorton D, Davis JN (1987) The distribution ofβ 1 andβ 2-adrenergic receptors of normal and reeler mouse brain: an in vitro autoradiographic study. Neuroscience 23:199–210

    Google Scholar 

  • Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437–470

    Google Scholar 

  • McElligot JG, Freedman W (1988a) Vestibulo-ocular reflex adaptation in cats before and after depletion of norepinephrine. Exp Brain Res 69:509–521

    Google Scholar 

  • McElligot JG, Freedman W (1988b) Central and cerebellar norepinephrine depletion and vestibulo-ocular reflex (VOR) adaptation. In: Flohr H (eds) Post-lesion neuronal plasticity. Springer, Berlin Heidelberg New York Tokyo, pp 661–674

    Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Google Scholar 

  • Minneman KP, Hegstrand LR, Molinoff PB (1979) Simultaneous determination ofβ 1 andβ 2-adrenergic receptors in tissues containing both receptor types. Mol Pharmacol 16:34–46

    Google Scholar 

  • Minneman KP, Pittman RN, Molinoff PB (1981)β-adrenergic receptor subtypes: properties, distribution and regulation. Annu Rev Neurosci 4:419–461

    Google Scholar 

  • Miyashita Y, Watanabe E (1984) Loss of vision-guided adaptation of the vestibulo-ocular reflex after depletion of brain serotonin in the rabbit. Neurosci Lett 51:177–182

    Google Scholar 

  • Myers RD (1966) Injection of solutions into cerebral tissue: relation between volume and diffusion. Physiol Behav 1:171–174

    Google Scholar 

  • Nagao S (1983) Effect of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic responses in pigmented rabbits. Exp Brain Res 53:36–46

    Google Scholar 

  • Olson L, Fuxe K (1971) On the projections from the locus coeruleus noradrenaline neurons: the cerebellar innervation. Brain Res 28:165–171

    Google Scholar 

  • Palacios JM, Kuhar MJ (1980)β-adrenergic receptor localization by light microscopic autoradiography. Science 208:1378–1380

    Google Scholar 

  • Palacios JM, Kuhar MJ (1982)β-adrenergic receptor localization in rat brain by light microscopic autoradiography. Neurochem Int 4:473–490

    Google Scholar 

  • Pompeiano M, Galbani P, Ronca-Testoni S (1989) Distribution ofβ-adrenergic receptors in different cortical and nuclear regions of cat cerebellum, as revealed by binding studies. Arch Ital Biol 127:115–132

    Google Scholar 

  • Pompeiano O (1988) Basic aspects of vestibulospinal function. In: Igarashi M, Nute KG (eds) Proceedings symposium on vestibular organs and altered force environment. NASA Space Biochemical Research Institute, Houston, pp 1–23

    Google Scholar 

  • Pompeiano O, d'Ascanio P, Horn E, Stampacchia G (1987) Effects of local injection of theα 2-adrenergic agonist clonidine into the locus coeruleus complex on the gain of vestibulospinal and cervicospinal reflexes in decerebrate cats. Arch Ital Biol 125:225–269

    Google Scholar 

  • Pompeiano O, Van Neerven J, Van Der Steen J, Collewijn H (1988) Effects of injection of noradrenergic and GABA-ergic substances in the flocculus on the gain of the VOR and OKN in the rabbit. Eur J Neurosci [Suppl] 1:6.2

    Google Scholar 

  • Rainbow TC, Parsons B, Wolfe BB (1984) Quantitative autoradiography ofβ 1 andβ 2-adrenergic receptors in rat brain. Proc Natl Acad Sci USA 81:1585–1589

    Google Scholar 

  • Schairer JO, Bennett MVL (1986a) Changes in gain of the vestibulo-ocular reflex induced by combined visual and vestibular stimulation in goldfish. Brain Res 373:164–176

    Google Scholar 

  • Schairer JO, Bennett MVL (1986b) Changes in gain of the vestibulo-ocular reflex induced by sinusoidal visual stimulation in goldfish. Brain Res 373:177–181

    Google Scholar 

  • Segal M, Pickel J, Bloom FE (1973) The projection of the nucleus locus coeruleus: an autoradiographic study. Life Sci 13:817–821

    Google Scholar 

  • Silberman EK, Vivaldi E, Garfield J, McCarley RW, Hobson JA (1960) Carbachol triggering of desynchronized sleep phenomena: enhancement via small volume infusions. Brain Res 191:215–224

    Google Scholar 

  • Simpson JI, Graf W, Leonard C (1981) The coordinate system of visual climbing fibers to the flocculus. In: Fuchs A, Becker W (eds) Progress in oculomotor research: developments in neuroscience, Vol 12. Elsevier, Amsterdam, pp 475–484

    Google Scholar 

  • Somana R, Walberg F (1978) The cerebellar projection from locus coeruleus as studied with retrograde transport of horseradish peroxidase in the cat. Anat Embryol 155:87–94

    Google Scholar 

  • Stampacchia G, d'Ascanio P, Horn E, Pompeiano O (1988) Gain regulation of the vestibulospinal reflex following microinjection of aβ-adrenergic agonist or antagonist into the locus coeruleus and the dorsal pontine reticular formation. Adv Otorhinolaryngol 41:134–141

    Google Scholar 

  • Sutin J, Minneman KP (1985) Adrenergicβ-receptors are not uniformly distributed in the cerebellar cortex. J Comp Neurol 236:547–554

    Google Scholar 

  • Waterhouse BD, Sessler FM, Cheng JT, Woodward JD, Azizi SA, Moises HC (1988) New evidence for a gating action of norepinephrine in central neuronal circuits of mammalian brain. Brain Res Bull 21:425–432

    Google Scholar 

  • Watson M, McElligott JG (1983) 6-OHDA induced effects upon the acquisition and performance of specific locomotor tasks in rats. Pharmacol Biochem Behav 18:927–934

    Google Scholar 

  • Watson M, McElligott JG (1984) Cerebellar norepinephrine depletion and impaired acquisition of specific locomotor tasks in rats. Brain Res 296:129–138

    Google Scholar 

  • Yamamoto Y, Ishikawa M, Tanaka C (1977) Catacholaminergic terminals in the developing and adult rat cerebellum. Brain Res 132:355–361

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology I, Erasmus University Rotterdam, P.O. Box 1738, NL-3000, DR Rotterdam, The Netherlands

    J. van Neerven, H. Collewijn & J. van der Steen

  2. Department of Physiology and Biochemistry, University of Pisa, Via S. Zeno 31, I-56100, Pisa, Italy

    O. Pompeiano

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  1. J. van Neerven
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  2. O. Pompeiano
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  3. H. Collewijn
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  4. J. van der Steen
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van Neerven, J., Pompeiano, O., Collewijn, H. et al. Injections of β-noradrenergic substances in the flocculus of rabbits affect adaptation of the VOR gain. Exp Brain Res 79, 249–260 (1990). https://doi.org/10.1007/BF00608233

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