Summary
A method has been developed for recording the response of single neurons in the lamprey brainstem in vitro to natural stimulation of vestibular receptors. The brainstem dissected together with the intact vestibular apparatus could be rotated in space, in two perpendicular planes (transverse, the roll tilt, and sagittal, the pitch tilt), in one of them up to 360°, and in the other one up to ± 30°. The responses of single reticulospinal (RS) neurons, in all four reticular nuclei of the brainstem, to roll and pitch were recorded extracellularly and, with small inclinations (up to ±45°) also intracellularly. Two types of preparations were used, with and without the rostral part of the spinal cord. In the brainstem preparations, most RS neurons responded both to a definite brain orientation in space and to a change of the orientation (static and dynamic reactions). Responses to roll tilt were similar in all reticular nuclei: all cells were excited with roll tilt towards the contralateral side, this reaction was qualitatively preserved when the roll was performed in combination with different pitch inclinations. Responses to pitch tilt were less clearcut; some neurons were activated with noseup deflection while others responded to nose-down tilt. In preparations including the spinal cord, responses of RS neurons to roll and pitch tilt differed from those in the isolated brainstem in that they were much less specific and sfable. Roll and pitch tilts could trigger the spinal locomotor CPG, which, by sending “efference copy” signals back to the brainstem, produced modulation of RS neurons in relation to the locomotor rhythm.
Similar content being viewed by others
References
Arshavsky Yul, Deliagina TG, Okshtein IL, Orlovsky GN, Panchin YuV (1990) Neuronal mechanisms of the defensive reaction to statocyst receptor stimulation in freshwater snail Planorbarius corneus. Nejrofiziologia 22: 795–803
Arshavsky YuI, Orlovsky GN, Panchin YuV (1991) Comparative study of vestibular control of posture and rhythmic movements. In: Shimamura M et al. (eds) Neurobiological basis of human locomotion. Jpn Scient Soc Press, pp 213–219
Brodin L, Grillner S, Dubuc R, Ohta Y, Kasicki S, Hökfelt T (1988) Reticulospinal neurons in lamprey: transmitters, synaptic interactions and their role during locomotion. Arch Ital Biol 126: 317–345
Burlet de HM, Versteegh C (1930) Ueber Bau und Funktion des Petromyzonlabyrinthes. Acta Oto-Laryngol Suppl 13: 5–58
Currie SN, Carlsen RC (1987a) Modulated vibration-sensitivity of lamprey mauthner neurons. J Exp Biol 129: 41–51
Currie SN, Carlsen RS (1987b) Functional significance and neural basis of larval lamprey startle behaviour. J Exp Biol 133: 121–135
Currie SN, Carlson RC (1988) Cranial components of startle behaviour in larval and adult lampreys. Neurosciences 24: 709–718
Deliagina TG, Orlovsky GN, Grillner S, Wallen P (1992a) Vestibular control of swimming in lamprey. II. Characteristics of spatial sensitivity of reticulospinal neurons. Exp Brain Res 90: 489–498
Deliagina TG, Orlovsky GN, Grillner S, Wallén P (1992b) Vestibular control of swimming in lamprey. III. Activity of vestibular afferents. Convergence of vestibular inputs on reticulospinal neurons. Exp Brain Res 90: 499–507
Dubuc R, Ohta Y, Grillner S (1988) Excitatory amino acid and GABA transmission to reticulospinal neurons in the lamprey. Soc Neurosci Abstr 14: 264
Dubuc R, Grillner S (1989) The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 483: 196–200
Fraser PJ, Bevengut M, Clarac F (1987) Swimming patterns and the activity of identified equilibrium interneurones in the shore crab, Carcinus maenas. J Exp Biol 130: 305–330
Gesteland RC, Howland B, Lettwin JY, Pitts WH (1959) Comments on microelectrodes. Proc Inst Radio Engng 47: 1856–1862
Harris JE (1936) The role of the fins in the equilibrium of the swimming fish. I. Wind-tunnel tests on a model of Mustelus canis (Mitchill). J Exp Biol 13: 476–493
Hill R, Århem P, Grillner S (1985) Ionic mechanisms of 3 types of functionally different neurons in the lamprey spinal cord. Brain Res 358: 40–52
Holst E (1950) Die Arbeitsweise des Statolithenapparates bei Fishen. Z Vergl Physiol 32: 60–120
Kasicki S, Grillner S (1986) Muller cells and other reticulospinal neurons are phasically active during fictive locomotion in the isolated nervous system of the lamprey. Neurosci Lett 69: 239–243
Kasicki S, Grillner S, Ohta Y, Dubuc R, Brodin L (1989) Phasic modulation of reticulospinal neurons during fictive locomotion and other types of motor activity in lamprey. Brain Res 484: 203–216
Koyama H, Kishida R, Goris RC, Kusunoki T (1989) Afferent and efferent projections of the VIIIth cranial nerve in the lamprey Lampetra japonica. J Comp Neurol 280: 663–671
McClellan AD (1988) Brainstem command systems for locomotion in the lamprey: localization of descending pathways in the spinal cord. Brain Res 457: 338–349
McClellan A, Grillner S (1984) Activation of “fictive swimming” by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey spinal cord. J Neurosci 8: 133–145
Mittelstaedt H (1975) On the processing of postural information. Forschr Zool 23: 128–141
Nieuwenhuys R (1972) Topological analysis of the brainstem of the lamprey Lampetra fluviatilis. J Comp Neurol 145: 165–178
Northcutt RG (1979) Central projections of the eight cranial nerve in lampreys. Brain Res 167: 163–167
Ohta Y, Grillner S (1989) Monosynaptic excitatory amino acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. J Neurophysiol 62: 1079–1089
Orlovsky GN (1969) Spontaneous and induced locomotion of the thalamic cat. Biofizika 14: 1154–1162
Orlovsky GN (1970) Work of the reticulo-spinal neurons during locomotion. Biofizika 15: 761–771
Orlovsky GN (1991) Gravistatic postural control in simpler systems. Current Biol 1: 612–627
Platt C (1983) The peripheral vestibular system of fish. In: Northcutt RG and Davis RE (eds) Fish neurobiology. Univ Michigan Press, pp 89–123
Rovainen CM (1967) Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). 1. Muller and Mauthner cells. J Neurophysiol30: 1000–1023
Rovainen CM (1974) Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. J Comp Neurol 154: 207–223
Rovainen CM (1979) Electrophysiology of vestibulospinal and vestibuloreticulospinal systems in lampreys. J Neurophysiol 42: 745–766
Rovainen CM (1982) Neurophysiology. In: MW Hardisty, JC Potter (eds) The biology of lamprey. Acad Press, New York, pp 1–136
Rovainen CM, Johnson PA, Roach EA, Mankovsky JA (1973) Projections of individual axons in lamprey spinal cord determined by tracings through serial sections. J Comp Neurol 149: 193–201
Rubinson K (1974) The central distribution of VIII nerve afferents in larval Petromyzon marinus. Brain Behav Evol 10: 121–129
Timerick SJB, Paul DH, Roberts BL (1990) Dynamic characteristics of vestibular-driven compensatory fin movements of the dogfish. Brain Res 516: 318–321
Vinay L, Matsushima T, Shupliakov O, Grillner S (1991) Identification of spinal neurons with ascending axons transmitting information about ongoing locomotor activity to the brain in lamprey. Abst Scand Physiol Soc in Uppsala P63
Wallen P, Grillner S, Feldman JL, Bergelt S (1985) Dorsal and ventral myotome motoneurons and their input during fictive locomotion in lamprey. J Neurosci 5: 654–661
Wickelgren W (1977) Physiological and anatomical characteristics of reticulospinal neurons in lamprey. J Physiol (Lond) 270: 89–114
Wilson VJ, Melvill Jones (1979) Mammalian Vestibular Physiology. Plenum Press, New York and London
Wilson VJ, Yamagata Y, Yates BI, Schor R, Nonaka S (1990) Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation. J Neurophysiol 64: 1695–1703
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Orlovsky, G.N., Deliagina, T.G. & Wallén, P. Vestibular control of swimming in lamprey. Exp Brain Res 90, 479–488 (1992). https://doi.org/10.1007/BF00230930
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00230930