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Experimental Brain Research

, Volume 57, Issue 1, pp 167–176 | Cite as

Projections from the superior colliculus to a region of the central mesencephalic reticular formation (cMRF) associated with horizontal saccadic eye movements

  • B. Cohen
  • J. A. Büttner-Ennever
Article

Summary

Radioactive wheatgerm agglutinin (WGA) and horseradish peroxidase (HRP) were injected into portions of the mesencephalic reticular formation at sites where electrical stimulation induced either small or large contralateral horizontal saccadic eye movements. We have designated this region as the Central MRF (cMRF). It contains both cells and fiber tracts, including the efferent output of the superior colliculus (SC), destined for the dorsal tegmental decussation and the predorsal bundle. Cells labelled by WGA and HRP injections were found in the intermediate and deep layers of the superior colliculus and the adjacent central gray matter on the ipsilateral side. Injections into the dorsal cMRF, at sites where small saccades were induced, caused labelling of cells in the rostral intermediate layer of SC. Injections into the ventral cMRF, at points where large saccades were elicited, caused labelling of cells in the caudal intermediate layer of SC. The deepest layers of SC and the adjacent central gray were also labelled from the small eye movement region of dorsal cMRF. We interpret these findings to indicate that the intermediate layers of SC send axonal projections to the horizontal eye movement region of the MRF in a topographic fashion. The projection from the intermediate layer is organized so that regions in SC and cMRF related to small or to large eye movements are interconnected. The results support the hypothesis that cMRF is a topographically organized area, involved, like SC, in the control of eye movements. Since both cMRF and the superior colliculus project to areas of the pons and medulla where saccadic eye movements are produced, they could give rise to parallel pathways for the generation of contralateral saccades.

Key words

Mesencephalic reticular formation Superior colliculus Oculomotor Saccades Horseradish peroxidase Wheatgerm agglutinin 

Abbreviations

III

oculomotor nucleus

IV

trochlear nucleus

ap

area pretectalis

BC

brachium conjunctivum

BSC

brachium of the superior colliculus

cg

central gray

cMRF

central MRF

d

deep layer of SC

DAB

diaminobenzidine

EOG

electro-oculography

h

habenula nuclei

HRP

horseradish peroxidase

iC

interstitial nucleus of Cajal

ic

inferior colliculus

li

nucleus limitans

mg

medial geniculate body

MLF

medial longitudinal fasciculus

nIII

oculomotor nerve

nIV

trochlear nerve

on

olivary nucleus

p

pulvinar

PC

posterior commissure

riMLF

rostral interstitial nucleus of the MLF

rn

red nucleus, pars magnocellularis

rnp

red nucleus, pars parvocellularis

s

superficial layer of SC

SC

superior colliculus

sl

sublentiform nucleus

sn

substantia nigra

TMB

tetramethyl benzidine

TR

tractus retroflexus

WGA

wheatgerm agglutinin

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References

  1. Baker R, Baker H, Blanchard J, Shaw M, Soriano D (1981) Antero- and retrograde transport of wheatgerm agglutinin following extra- and intracellular injection in the cat vestibulo-oculomotor system. Soc Neurosci Abstr 7: 489Google Scholar
  2. Bender MB, Shanzer S (1964) Oculomotor pathways defined by electric stimulation and lesions in the brainstem of monkeys. In: Bender MB (ed) The oculomotor system. Harper & Row, New York, pp 81–140Google Scholar
  3. Benevento LA, Fallon JH (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J Comp Neur 160: 339–362Google Scholar
  4. Bolton AE (1979) Radioiodination Techniques. The Radiochemical Centre Ltd., Amersham Bucks, EnglandGoogle Scholar
  5. Büttner-Ennever JA, Grob P, Akert K, Bizzini B (1981) Transynaptic retrograde labelling in the oculomotor system of the monkey with (125I) tetanus toxin BIIb fragment. Neurosci Lett 26: 233–238Google Scholar
  6. Cohen B, Büttner-Ennever J, Waitzman D, Bender MB (1981) Anatomical connections of a portion of the dorsolateral mesencephalic reticular formation of the monkey associated with horizontal saccadic eye movements. Soc Neurosci Abstr 7: 132Google Scholar
  7. Cohen B, Matsuo V, Raphan T, Waitzman D, Fradin J (1982) Horizontal saccades induced by stimulation of the mesencephalic reticular formation. In: Roucoux A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. Dr W Junk Publishers, The Hague, Boston, London pp 325–335Google Scholar
  8. Crosby EC, Woodburne RT (1943) The nuclear pattern of the non-tectal portions of the midbrain and isthmus in primates. JComp Neurol 78: 441–481Google Scholar
  9. Edwards SB (1975) Autoradiographic studies of the projections of the midbrain reticular formation: descending projections of nucleus cuneiformis. J Comp Neurol 161: 341–358Google Scholar
  10. Edwards SB, Henkel CK (1978) Superior colliculus connections with the extraocular motor nuclei in the cat. J Comp Neurol 179: 451–468Google Scholar
  11. Edwards SB (1980) The deep cell layers of the superior colliculus: Their reticular characteristics and structural organization. In: Hobson JA, Brazier MD (eds) The Reticular Formation Revisited. Raven Press, New York, pp 193–209Google Scholar
  12. Edwards SB, deOlmos JS (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projections of nucleus cuneiformis. J Comp Neurol 165: 417–432Google Scholar
  13. Feremutsch K (1965) Mesencephalon. In: Hofer H, Schultz AH, Stark D (eds) Primatologia. Handbuch der Primatenkunde Vol II/2, Karger, Basel, pp 1–174Google Scholar
  14. Forel A (1877) Untersuchungen über die Haubenregion und ihre oberen Verknüpfungen im Gehirn des Menschen und einiger Säugetiere mit Beiträgen zu den Methoden der Gehirnuntersuchung. Arch Psychiat 7: 393–493Google Scholar
  15. Graham RC Jr, Karnovski MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney; ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14: 291–302Google Scholar
  16. Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbar-spinal tract. Exp Brain Res 46: 243–256Google Scholar
  17. Grob P, Büttner-Ennever J, Lang W, Akert K, Fäh A (1982) A comparison of the retrograde tracer properties of (125I) wheat germ agglutinin (WGA) with HRP after injection into the corpus callosum. Brain Res 236: 193–198Google Scholar
  18. Guitton D, Crommelinck M, Roucoux A (1980) Stimulation of the superior colliculus in the alert cat. I. Eye movements and neck EMG activity evoked when the head is restrained. Exp Brain Res 39: 63–73Google Scholar
  19. Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 166: 133–144Google Scholar
  20. Harting JK, Huerta MF, Frankfurter AJ, Strominger NL, Royce GJ (1980) Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J Comp Neurol 192: 853–882Google Scholar
  21. Komatsuzaki A, Alpert J, Harris HE, Cohen B (1972) Effects of mesencephalic reticular formation lesions on optokinetic nystagmus. Exp Neurol 34: 522–534Google Scholar
  22. Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurochemistry: a non carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26: 106–117PubMedGoogle Scholar
  23. Mesulam M-M (1982) Principles of HRP neurochemistry and their applications for tracing neural pathways: axonal transport, enzyme histochemistry and light microscopic analysis. In: Mesulam M-M (ed) Tracing neural connections with horseradish peroxidase. John Wiley and Sons, New York, p 68Google Scholar
  24. Olszewski J, Baxter D (1954) Cytoarchitecture of the human brain stem. Karger, Basel pp 1–199Google Scholar
  25. Raphan T, Cohen B (1978) Brainstem mechanisms for rapid and slow eye movements. Ann Rev Physiol 40: 527–552Google Scholar
  26. Raybourn MS, Keller EL (1977) Colliculo-reticular organization in primate oculomotor system. J Neurophysiol 40: 861–878Google Scholar
  27. Robinson DA (1982) Eye movements evoked by superior collicular stimulation in the alert monkey. Vision Res 12: 1795–1808Google Scholar
  28. Roucoux A, Guitton D, Crommelinck M (1980) Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp Brain Res 39: 75–85Google Scholar
  29. Schiller PH, Stryker M (1972) Single unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35: 915–924Google Scholar
  30. Schiller PH, True SD, Conway JL (1980) Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol 44: 1175–1189PubMedGoogle Scholar
  31. Shantha TR, Manocha SL, Bourne GHI (1968) Stereotaxic atlas of the Java monkey brain (Macaca iris). The Williams and Wilkins Co, Baltimore, MarylandGoogle Scholar
  32. Stern K (1936) Der Zellaufbau des menschlichen Mittelhirns. Mit einem histopathologischen Anhang. In: Förster O, Gaupp R, Rüdin E (eds) Zeitschrift für die gesamte Neurologie und Psychiatrie. Springer, Berlin, pp 520–598Google Scholar
  33. Stöckel K, Paravicini U, Thönen H (1974) Specificity of the retrograde axonal transport of nerve growth factor. Brain Res 76: 413–421Google Scholar
  34. Szentágothai J (1943) Die zentrale Innervation der Augenbewegungen. Arch Psychiatr Nervenkr 110: 721–760Google Scholar
  35. Taber E (1961) The cytoarchitecture of the brain stem of the cat. I. Brain stem nuclei of cat. J Comp Neurol 116: 27–69Google Scholar
  36. Waitzman D (1982) Burst neurons in the mesencephalic reticular formation (MRF) associated with visually-targeted and spontaneous saccades, Ph.D. Thesis, City University of New YorkGoogle Scholar
  37. Waitzman D, Cohen B (1979) Unit activity in the mesencephalic reticular formation (MRF) associated with saccades and positions of fixation during a visual attention task. Soc Neurosci Abstr 5: 389Google Scholar
  38. Weber J, Harting JK (1980) The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis. Brain Res 194: 1–2PGoogle Scholar
  39. Wurtz RH, Albano JE (1980) Visual-motor function of the primate superior colliculus. Ann Rev Neurosci 3: 189–226Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • B. Cohen
    • 1
  • J. A. Büttner-Ennever
    • 1
    • 2
  1. 1.Department of NeurologyMount Sinai School of Medicine of the City University of New YorkNew YorkUSA
  2. 2.the Institute of Anatomy, University of DüsseldorfDüsseldorfFederal Republic of Germany

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