Summary
Interaction of semicircular canal and neck proprioceptive inputs was studied in the cerebral cortex of awake, intact cats. Neuronal responses were recorded extracellularly in the anterior suprasylvian gyrus of the left hemisphere. Stimulations consisted of horizontal rotations in the dark applied as sinusoids or position ramps. There were three stimulus conditions: (1) Pure canal stimulation; rotation of whole body. (2) Pure neck stimulation; rotation of trunk about stationary head. (3) Canalneck interaction; rotation of head about stationary trunk.
(1) We recorded 105 neurons with either Type I or Type II canal response. These showed often pronounced non-linearities such as a clear firing increase upon rotation in the “on-direction” and hardly any decrease in the opposite direction. The responses reflected mostly angular velocity, but angular position signals were also obtained. (2) In 79 neurons, either Type I or Type II neck responses were obtained. They coded either angular velocity, velocity plus position, or position. (3) Canal-neck convergence was found in 67 of 88 neurons tested. In the majority of neurons, interaction was “dantagonistic” in the sense that the canal and neck responses tended to cancel each other during rotation of the head about the stationary trunk. These neurons could signal trunk rotation in space rather than head in space or head relative to trunk. Most of the remaining neurons showed a “synergistic” interaction such that the response upon head rotation was enhanced as compared to whole body or trunk rotation. These neurons might be involved in the dual task of monitoring head rotation in space and relative to trunk. Interaction was compatible with linear summation of canal and neck inputs in 70% of the neurons. In part of these, however, the assumption had to be made that the interaction had taken place already at some stage prior to the cortical neurons investigated. The response characteristics of cortical canal neurons are discussed in comparison to vestibular nuclear neurons. Furthermore, parallels are drawn between the observed canal-neck interactions in the cortical neurons and (i) interactions of canal and neck dependent postural reflexes in the decerebrate cat, and (ii) interactions of canal and neck induced turning sensations in man.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Anastasopoulos D, Mergner T (1982) Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res 46: 269–280
Andersson S, Gernandt BE (1954) Cortical projection of vestibular nerve in cat. Acta Oto-laryngol (Stockh) Suppl 116: 10–18
Becker W, Deecke L, Mergner T (1979) Neuronal responses to natural vestibular and neck stimulation in the anterior suprasylvian gyrus of the cat. Brain Res 165: 139–143
Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45: 852–868
Büttner U, Buettner UW (1978) Parietal cortex (2v) neuronal activity in the alert monkey during natural vestibular and optokinetic stimulation. Brain Res 153: 392–397
Büttner U, Waespe W (1981) Vestibular nerve activity in the alert monkey during vestibular and optokinetic nystagmus. Exp Brain Res 41: 310–315
Büttner U, Henn V, Oswald HP (1977) Vestibular-related neuronal activity in the thalamus of the alert monkey during sinusoidal rotation in the dark. Exp Brain Res 30: 435–444
Buettner UW, Büttner U, Henn V (1978) Transfer characteristics of neurons in the vestibular nuclei of the alert monkey. J Neurophysiol 41: 1614–1628
Copack P, Dafny N, Gilman S (1972) Neurophysiological evidence of vestibular projections to thalamus, basal ganglia, and cerebral cortex. In: Frigyesi T, Rinvik E, Yahr MD (eds) Corticothalamic projections and sensorimotor acitivities. Raven, New York, pp 309–339
Deecke L, Becker W, Jürgens R, Mergner T (1979) Interaction of vestibular and somatosensory afferents for perception and postural control. Agressologie 20C: 179–184
Duensing F, Schaefer KP (1958) Die Aktivität einzelner Neurone im Bereich der Vestibulariskerne bei Horizontalbeschleuni gungen unter besonderer Berücksichtigung des vestibulären Nystagmus. Arch Psychiat Nervenkr 198: 225–252
Ezure K, Wilson VJ (1984) Interaction of tonic neck and vestibular reflexes in the forelimb of the decerebrate cat. Exp Brain Res 54: 289–292
Ezure K, Schor RH, Yoshida K (1978) The response of horizontal semicircular canal afferents to sinusoidal rotation in the cat. Exp Brain Res 33: 27–39
Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34: 635–660
Grüsser O-J, Pause M, Schreiter U (1982) Neuronal responses in the parieto-insular vestibular cortex of alert Java monkeys (Maccaca fascicularis). In: Roucoux A, Crommelink M (eds) Physiological and pathological aspects of eye movements. Dr W Junk, The Hague Boston London, pp 251–270
von Holst E, Mittelstaedt H (1950) Das Reafferenzprinzip (Wechselwirkungen zwischen Zentralnervensystem und Peripherie). Naturwissenschaften 37: 464–476
Keller EL, Precht W (1979) Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms. J Neurophysiol 42: 896–911
Kempinsky WH (1951) Cortical projection of vestibular and facial nerves in cat. J Neurophysiol 14: 203–210
Kornhuber HH (1966) Physiologie and Klinik des Zentralvestibulären Systems (Blick und Stützmotorik) In: Berendes J, Link R, Zöllner F (eds) Hals-Nasen-Ohren-Heilkunde III/3. Thieme, Stuttgart, pp 2150–2351
Kornhuber HH, da Fonseca JS (1964) Optovestibular integration in the cats cortex: a study of sensory convergence on cortical neurons. In: Bender MB (ed) The oculomotor system. Hoeber, New York, pp 239–279
Landgren S, Silfvenius H, Wolsk D (1967) Vestibular, cochlear, and trigeminal projections to the cortex in the anterior suprasylvian sulcus of the cat. J Physiol (Lond) 191: 561–573
Lindsay KW, Roberts TDM, Rosenberg JR (1976) Asymmetric tonic labyrinthine reflexes and their interaction with neck reflexes in the decerebrate cat. J Physiol (Lond) 261: 583–601
Massopust LC, Daigle HJ (1960) Cortical projection of the medial and spinal vestibular nuclei in the cat. Exp Neurol 2: 179–185
Mergner T, Anastasopoulos D, Becker W, Deecke L (1981a) Comparison of the modes of interaction of labyrinthine and neck afferents in the suprasylvian cortex and vestibular nuclei of the cat. In: Fuchs A, Becker W (eds) Progress in oculomotor research. Elsevier/North-Holland, New York, pp 343–350
Mergner T, Deecke L, Wagner H-J (1981b) Vestibulo-thalamic projection to the anterior suprasylvian cortex of the cat. Exp Brain Res 44: 455–458
Mergner T, Anastasopoulos D, Becker W (1982) Neuronal responses to horizontal neck deflection in the group x region of the cat's medullary brainstem. Exp Brain Res 45: 196–206
Mergner T, Nardi GL, Becker W, Deecke L (1983) The role of canal-neck interaction for the perception of horizontal trunk and head rotation. Exp Brain Res 49: 198–208
Mickle WA, Ades HW (1952) A composite sensory projection area in the cerebral cortex of the cat. Am J Physiol 170: 682–689
Mills KR, Taylor A (1974) The projection of the vestibular nerve to the cerebral cortex in the cat. J Physiol (Lond) 239: 165–178
Milojevic B, St. Laurent J (1966) Cortical vestibular projection in the cat. Aerospace Med 37: 709–712
Morzorati L, Barnes CD (1977) Sensitivity of components of the central vestibular complex to pentobarbital. Neuropharmacology 16: 295–298
Peterson BW, Bilotto G, Fuller JH, Goldberg J, Leeman B (1981a) Interaction of vestibular and neck reflexes in the control of gaze. In: Fuchs AF, Becker W (eds) Progress in oculomotor research. Elsevier/North Holland, New York, pp 335–342
Peterson BW, Bilotto G, Fuller JH, Goldberg J, Wilson VJ (1981b) Dynamics of vestibulo-ocular, vestibulo-collic, and cervico-collic reflexes. Ann NY Acad Sci 374: 395–402
Roberts TDM (1973) Reflex balance. Nature 244: 156–158
Robinson DA (1975) Oculomotor control signals. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon, Oxford, pp: 337–374
Roucoux-Hanus M, Boisacq-Schepens N (1974) Projections vestibulaires au niveau des aires corticales suprasylvienne et postcruciée chez le Chat anesthesié au chloralose. Arch ital Biol 112: 60–76
Sans A, Raymond J, Marty R (1970) Responses thalamiques et corticales à la stimulation èlectrique du nerf vestibulaire chez le Chat. Exp Brain Res 10: 265–275
Sestokas AK (1980) Response characteristics of vestibulo-cortical neurons to rotations of the cat in the dark and light. Soc Neurosci Abstr 6: 559
Spiegel EA, Szekely EG, Gildenberg PL (1965) Vestibular responses in midbrain, thalamus, and basal ganglia. Arch Neurol 12: 258–269
Stevens JK, Emerson RC, Gerstein GL, Kallos T, Neufeld GR, Nichols CW, Rosenquist AC (1976) Paralysis of the awake human: visual perception. Vision Res 16: 93–98
Tomko DL, Barbaro NM, Ali FN (1981) Effect of body tilt on receptive field orientation of simple visual cortical neurons in unanesthetized cats. Exp Brain Res 43: 309–314
Unna KR, Pelikan EW, Macfarlane DW, Cazort RJ, Sadove MS, Nelson JT (1950) Evaluation of curarizing agents in man. J Am Med Ass 144: 448–451
Walzl EM and Mountcastle VB (1949) Projection of vestibular nerve to cerebral cortex of the cat. Am J Physiol 159: 595
Watanabe S, Jijiwa H, Itoh K (1975) Responses of cortical vestibular center produced by stimulation of vestibular nuclei and visual association area in the cat. Acta Otolaryngol (Suppl) 330: 147–158
Werner G, Whitsel BL (1968) Topology of the body representation in somatosensory area I of primates. J Neurophysiol 31: 856–869
Wilson VJ, Ezure K, Timerick SJB (1984) Tonic neck reflex of the dererebrate cat: Response of spinal interneurons to natural stimulation of neck and vestibular receptors. J Neurophysiol 51: 567–577
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mergner, T., Becker, W. & Deecke, L. Canal-neck interaction in vestibular neurons of the cat's cerebral cortex. Exp Brain Res 61, 94–108 (1985). https://doi.org/10.1007/BF00235625
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00235625