Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1980 Jan;298:85–110. doi: 10.1113/jphysiol.1980.sp013069

Interactions between extraocular proprioceptive and visual signals in the superior colliculus of the cat.

I M Donaldson, A C Long
PMCID: PMC1279104  PMID: 7359446

Abstract

1. The responses of units in the superficial layers of the superior colliculus to stretch of extrinsic ocular muscles (e.o.m.) and to visual stimuli, delivered singly and paired at various inter-stimulus intervals, were studied in chloralose-anaesthetized cats. 2. Most units responded to visual stimuli and about half also gave phasic excitatory responses to stretch of e.o.m. 3. Signals from the e.o.m. of each eye reach both superior colliculi; only those in the colliculus ipsilateral to the e.o.m. stretched were studied in detail. 4. A variety of control experiments provided evidence that the signal leading to the responses to e.o.m. stretch was extraretinal. The strong probability is that the receptors responsible were in the extrinsic ocular muscles or their tendons. 5. Of fifty-six units, twenty-four (43%) showed definite interactions between the effects of visual stimuli delivered to the left eye and those due to stretch of e.o.m. of the right eye whose retina had been destroyed. 6. Interactions were found with both stationary and moving visual stimuli. They involved either enhancement or reduction (sometimes abolition) of the response to either e.o.m. or visual stimulation, particularly the latter. 7. Units with interactions showed one of three types of behaviour. (1) Excitatory responses to visual and e.o.m. stimuli given singly, and interactions when the two types of stimulus were paired at some time intervals. Suppression and abolition of visual responses by preceding e.o.m. stretch was common. (2) Units with little or no excitatory response to e.o.m. stretch applied alone, but with showed reduction of their visual responses by preceding e.o.m. stretch. (3) Units with minimal responses to either type of stimulus presented alone but which gave markedly enhanced responses when visual and e.o.m. stimuli were paired. 8. These interactions between proprioceptive and retinal signals are thought to allow retinal image movements which result from saccades to be distinguished from those due to movement of objects in the external world.

Full text

PDF
89

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahams V. C., Rose P. K. Projections of extraocular, neck muscle, and retinal afferents to superior colliculus in the cat: their connections to cells of origin of tectospinal tract. J Neurophysiol. 1975 Jan;38(1):10–18. doi: 10.1152/jn.1975.38.1.10. [DOI] [PubMed] [Google Scholar]
  2. Batini C., Horcholle-Bossavit G. Interaction entre activation visuelle et activation proprioceptive au niveau des neurones du colliculus supérieur. C R Acad Sci Hebd Seances Acad Sci D. 1977 Dec 19;285(16):1491–1493. [PubMed] [Google Scholar]
  3. Buisseret P., Maffei L. Extraocular proprioceptive projections to the visual cortex. Exp Brain Res. 1977 Jun 27;28(3-4):421–425. doi: 10.1007/BF00235720. [DOI] [PubMed] [Google Scholar]
  4. COOPER S., DANIEL P. M., WHITTERIDGE D. Nerve impulses in the brainstem of the goat; responses with long latencies obtained by stretching the extrinsic eye muscles. J Physiol. 1953 Jun 29;120(4):491–513. doi: 10.1113/jphysiol.1953.sp004913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. COOPER S., DANIEL P. M., WHITTERIDGE D. Nerve impulses in the brainstem of the goat; short latency responses obtained by stretching the extrinsic eye muscles and the jaw muscles. J Physiol. 1953 Jun 29;120(4):471–490. doi: 10.1113/jphysiol.1953.sp004912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. COOPER S., FILLENZ M. Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles. J Physiol. 1955 Feb 28;127(2):400–413. doi: 10.1113/jphysiol.1955.sp005266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Campbell F. W., Wurtz R. H. Saccadic omission: why we do not see a grey-out during a saccadic eye movement. Vision Res. 1978;18(10):1297–1303. doi: 10.1016/0042-6989(78)90219-5. [DOI] [PubMed] [Google Scholar]
  8. Corfield R., Frosdick J. P., Campbell F. W. Grey-out elimination: the roles of spatial waveform, frequency and phase. Vision Res. 1978;18(10):1305–1311. doi: 10.1016/0042-6989(78)90220-1. [DOI] [PubMed] [Google Scholar]
  9. Donaldson I. M., Hawthorne M. E. Use of a small computer on-line to examine cerebellar visual responses [proceedings]. J Physiol. 1976 Sep;260(2):3P–3P. [PubMed] [Google Scholar]
  10. Donaldson I. M., Long A. C. Suppression of visual responses in the cat superior colliculus following stretch of extraocular muscles [proceedings]. J Physiol. 1977 Oct;272(1):94P–95P. [PubMed] [Google Scholar]
  11. Donaldson I. M., Nash J. R. Variability of the relative preference for stimulus orientation and direction of movement in some units of the cat visual cortex (areas 17 and 18). J Physiol. 1975 Feb;245(2):305–324. doi: 10.1113/jphysiol.1975.sp010847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Feldon P., Kruger L. Topography of the retinal projection upon the superior colliculus of the cat. Vision Res. 1970 Feb;10(2):135–143. doi: 10.1016/0042-6989(70)90111-2. [DOI] [PubMed] [Google Scholar]
  13. Henry G. H., Bishop P. O., Tupper R. M., Dreher B. Orientation specificity and response variability of cells in the striate cortex. Vision Res. 1973 Sep;13(9):1771–1779. doi: 10.1016/0042-6989(73)90094-1. [DOI] [PubMed] [Google Scholar]
  14. Maier A., DeSantis M., Eldred E. The occurrence of muscle spindles in extraocular muscles of various vertebrates. J Morphol. 1974 Aug;143(4):397–408. doi: 10.1002/jmor.1051430404. [DOI] [PubMed] [Google Scholar]
  15. Manni E., Palmieri G., Marini R. Mesodiencephalic representation of the eye muscle proprioception. Exp Neurol. 1972 Nov;37(2):412–421. doi: 10.1016/0014-4886(72)90084-2. [DOI] [PubMed] [Google Scholar]
  16. Merrill E. G., Ainsworth A. Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng. 1972 Sep;10(5):662–672. doi: 10.1007/BF02476084. [DOI] [PubMed] [Google Scholar]
  17. Nikara T., Bishop P. O., Pettigrew J. D. Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Exp Brain Res. 1968;6(4):353–372. doi: 10.1007/BF00233184. [DOI] [PubMed] [Google Scholar]
  18. Robinson D. A. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 1972 Nov;12(11):1795–1808. doi: 10.1016/0042-6989(72)90070-3. [DOI] [PubMed] [Google Scholar]
  19. Robinson D. L., Wurtz R. H. Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. J Neurophysiol. 1976 Jul;39(4):852–870. doi: 10.1152/jn.1976.39.4.852. [DOI] [PubMed] [Google Scholar]
  20. Rose P. K., Abrahams V. C. The effect of passive eye movement on unit discharge in the superior colliculus of the cat. Brain Res. 1975 Oct 24;97(1):95–106. doi: 10.1016/0006-8993(75)90916-6. [DOI] [PubMed] [Google Scholar]
  21. Skavenski A. A. Inflow as a source of extraretinal eye position information. Vision Res. 1972 Feb;12(2):221–229. doi: 10.1016/0042-6989(72)90113-7. [DOI] [PubMed] [Google Scholar]
  22. Stein B. E., Magalhães-Castro B., Kruger L. Relationship between visual and tactile representations in cat superior colliculus. J Neurophysiol. 1976 Mar;39(2):401–419. doi: 10.1152/jn.1976.39.2.401. [DOI] [PubMed] [Google Scholar]
  23. Straschill M., Hoffmann K. P. Activity of movement sensitive neurons of the cat's tectum opticum during spontaneous eye movements. Exp Brain Res. 1970;11(3):318–326. doi: 10.1007/BF01474390. [DOI] [PubMed] [Google Scholar]
  24. Straschill M., Rieger P. Eye movements evoked by focal stimulation of the cat's superior colliculus. Brain Res. 1973 Sep 14;59:211–227. doi: 10.1016/0006-8993(73)90262-x. [DOI] [PubMed] [Google Scholar]
  25. Syka J., Radil-Weiss T. Electrical stimulation of the tectum in freely moving cats. Brain Res. 1971 May 21;28(3):567–572. doi: 10.1016/0006-8993(71)90068-0. [DOI] [PubMed] [Google Scholar]
  26. WHITTERIDGE D. The effect of stimulation of intrafusal muscle fibres on sensitivity to stretch of extraocular muscle spindles. Q J Exp Physiol Cogn Med Sci. 1959 Oct;44:385–393. doi: 10.1113/expphysiol.1959.sp001420. [DOI] [PubMed] [Google Scholar]
  27. Wurtz R. H., Goldberg M. E. Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. J Neurophysiol. 1972 Jul;35(4):575–586. doi: 10.1152/jn.1972.35.4.575. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES