Skip to main content
SpringerLink
Log in

The projection from superior colliculus to cuneiform area in the rat

I. Anatomical studies

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Although the ipsilateral descending pathway is a major output projection of the superior colliculus, little is known of its functions. We therefore carried out two studies to investigate in rats the part of the ipsilateral projection that terminates in an area ventral to the inferior colliculus, referred to as the cuneiform nucleus. The first study, described here, used orthograde and retrograde tract-tracing techniques to locate the cells of origin and precise region of termination of the tectocuneiform pathway. The main findings were as follows. Injections of WGA-HRP into the superior colliculus gave terminal label in the cuneiform nucleus and also in surrounding structures which included central grey, the mid-brain tegmentum bordering the parabigeminal nucleus, and the external nucleus of the inferior colliculus. As well as the strong ipsilateral projection, there was a much weaker contralateral one which crossed the midline in the tectal commissure. Label in the cuneiform nucleus was heaviest after injections into the medial deep layers. However, no clear evidence was found for topography within the tectocuneiform projection: cuneiform label varied in intensity rather than pattern of distribution with variation in the collicular location of the injection site. Injections of retrograde tracers into the cuneiform are a labelled large numbers of collicular cells, which were distributed mainly in the deep and intermediate grey layers. In agreement with the data from orthograde tracing, the heaviest concentration of labelled cells was found in the medial deep layers. This concentration extended into the adjacent dorsolateral part of central grey. A similar distribution of labelled cells was seen after injections into the structures next to the cuneiform nucleus that also receive a tectal projection. Comparison of this distribution with that obtained from injections into other parts of the ipsilateral projection, including dorsolateral basilar pons, suggested that the projection to the cuneiform area may arise from a distinct set of collicular output cells. The projection from the superior colliculus to the cuneiform nucleus and immediately adjacent areas may therefore be also functionally distinct, mediating a particular kind of tectally-elicited response. The lack of clear topography in the projection suggests that this response may not have precise spatial direction. Other connections of the cuneiform nucleus, for example its input from lamina I cells in the dorsal horn of the spinal cord, and its reciprocal connections with dorsolateral central grey, raise the possibility that the cuneiform nucleus could be involved in some form of defensive response to painful or threatening stimulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson ME, Yoshida M, Wilson VJ (1971) Influence of superior colliculus on cat neck motoneurons. J Neurophysiol 35: 462–470

    Google Scholar 

  • Arnault P, Roger M (1987) The connections of the peripeduncular area studied by retrograde and anterograde transport in the rat. J Comp Neurol 258: 463–476

    Google Scholar 

  • Beitz AJ (1982a) The sites of origin of brain stem neurotensin and serotonin projections to the rodent nucleus raphe magnus. J Neurosci 2: 829–842

    Google Scholar 

  • Beitz AJ (1982b) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7: 133–159

    Google Scholar 

  • Berthoz A, Grantyn A (1986) Neuronal mechanisms underlying eye-head coordination. In: Freund H-J, Büttner U, Cohen B, Noth J (eds) The oculomotor and skeletalmotor systems: differences and similarities. Elsevier, Amsterdam, pp 325–343

    Google Scholar 

  • Brodal P, Dietrichs E, Bjaalie JG, Nordby T, Walberg F (1983) Is lectin-coupled horseradish peroxidase taken up and transported by undamaged as well as damaged fibres in the central nervous system? Brain Res 278: 1–9

    Google Scholar 

  • Burne RA, Azizi SA, Mihailoff GA, Woodward DJ (1981) The tectopontine projection in the rat with comments on visual pathways to the basilar pons. J Comp Neurol 202: 287–307

    Google Scholar 

  • Carlton SM, Leichnetz GR, Young EG, Mayer DJ (1983) Supramedullary afferents of the nucleus raphe magnus in the rat: a study using the transcannula HRP gel and autoradiographic techniques. J Comp Neurol 214: 43–58

    Google Scholar 

  • Castaldi L (1923) Studi sulla struttura sulla sviluppo del mesencefalo: richerche in Cavia cobaya, Parte 1. Arch Ital Anat Embriol 20: 23–225

    Google Scholar 

  • Castaldi L (1926) Studi sulla struttura sulla sviluppo del mesencefalo: richerche in Cavia cobaya, Parte 3. Arch Ital Anat Embriol 23: 481–609

    Google Scholar 

  • Dacey DM, Ulinski PS (1986) Optic tectum of the eastern snake, Thamnophis sirtalis. II. Morphology of efferent cells. J Comp Neurol 245: 198–237

    Google Scholar 

  • Dean P, Redgrave P (1984) The superior colliculus and visual neglect in rat and hamster. III. Functional implications. Brain Res Rev 8: 155–163

    Google Scholar 

  • Dean P, Mitchell IJ, Redgrave P (1988a) Contralateral head movements produced by microinjection of glutamate into superior colliculus of rats: evidence for mediation by multiple output pathways. Neuroscience 24: 491–500

    Google Scholar 

  • Dean P, Mitchell IJ, Redgrave P (1988b) Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24: 501–510

    Google Scholar 

  • Dean P, Redgrave P, Mitchell IJ (1988c) Organisation of efferent projections from superior colliculus to brainstem in rat: evidence for functional output channels. In: Hicks TP, Benedek G (eds) Vision within extrageniculo-striate systems. Progress in brain research, Vol 77. Elsevier, Amsterdam (in press)

    CAS  Google Scholar 

  • Dean P, Redgrave P, Sahibzada N, Tsuji K (1986) Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19: 367–380

    Google Scholar 

  • Edwards SB (1980) The deep cells of the superior colliculus: their reticular characteristics and structural organization. In: Hobson JA, Brazier MAB (eds) The reticular formation revisited. Raven Press, New York, pp 193–209

    Google Scholar 

  • Fallon JH, Leslie FM (1986) Distribution of dynorphin and enkephalin peptides in the rat brain. J Comp Neurol 249: 293–336

    Google Scholar 

  • Garcia-Rill E (1986) The basal ganglia and the locomotor regions. Brain Res Rev 11: 47–63

    Google Scholar 

  • Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 290: 219–238

    Google Scholar 

  • Gerfen CR, Staines WA, Arbuthnott GW, Fibiger HC (1982) Crossed connections of the substantia nigra in rat. J Comp Neurol 207: 283–303

    Google Scholar 

  • Gibson RA, Hansma DI, Houk JC, Robinson FR (1984) A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Res 298: 235–241

    Google Scholar 

  • Graham J (1977) An autoradiographic study of the efferent connections of the superior colliculus in the cat. J Comp Neurol 173: 629–654

    Google Scholar 

  • Grantyn A, Grantyn R (1980) Reticular substrates for coordination of horizontal eye movements and their relation to tectal efferent pathways. In: Hobson JA, Brazier MAB (eds) The reticular formation revisited. Raven Press, New York, pp 211–225

    Google Scholar 

  • Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Exp Brain Res 46: 243–256

    Google Scholar 

  • Hall WC, May PJ (1984) The anatomical basis for sensorimotor transformations in the superior colliculus. In: Neff WD (ed) Contributions to sensory physiology, Vol 8. Academic Press, Orlando, pp 1–40

    Google Scholar 

  • Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173: 583–612

    Google Scholar 

  • Harting JK, Hall WC, Diamond IT, Martin GF (1973) Anterograde degeneration study of the superior colliculus in Tupaia glis: evidence for a subdivision between superficial and deep layers. J Comp Neurol 148: 361–386

    Google Scholar 

  • Harting JK, Huerta MF (1984) The mammalian superior colliculus: studies of its morphology and connections. In: Vanegas H (ed) The comparative neurology of the optic tectum. Plenum Press, New York, pp 687–773

    Google Scholar 

  • Henkel CK, Edwards SB (1978) The superior colliculus control of pinna movements in the cat: possible anatomical connections. J Comp Neurol 182: 763–776

    Google Scholar 

  • Holcombe V, Hall WC (1981a) The laminar origin and distribution of the crossed tectoreticular pathways. J Neurosci 1: 1103–1112

    Google Scholar 

  • Holcombe V, Hall WC (1981b) Laminar origin of ipsilateral tectopontine pathways. Neuroscience 6: 255–260

    Google Scholar 

  • Holstege G, Collewijn H (1982) The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J Comp Neurol 209: 139–175

    Google Scholar 

  • Huerta MF, Harting JK (1982) Tectal control of spinal cord activity: neuroanatomical demonstration of pathways connecting the superior colliculus with the cervical spinal cord grey. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progress in brain research, Vol 57. Elsevier, Amsterdam, pp 293–328

    Google Scholar 

  • Huerta MF, Harting JK (1984) Connectional organization of the superior colliculus. Trends Neurosci 7: 286–289

    Google Scholar 

  • Illing R-B, Graybiel AM (1986) Complementary and non-matching afferent compartments in the cat's superior colliculus: innervation of the acetylcholinesterase-poor domain of the intermediate gray layer. Neuroscience 18: 373–394

    Google Scholar 

  • Ingle DJ (1983) Brain mechanisms of visual localization by frogs and toads. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 177–226

    Google Scholar 

  • Keller EL (1979) Colliculoreticular organization in the oculomotor system. In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Progress in brain research, Vol 50, Elsevier, Amsterdam, pp 725–734

    Google Scholar 

  • Martin GF (1969) Efferent tectal pathways of the opossum (Didelphis virginiana). J Comp Neurol 135: 209–224

    Google Scholar 

  • May PJ, Hall WC (1984) Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. J Comp Neurol 226: 357–376

    Google Scholar 

  • May PJ, Vidal P-P, Baker R (1985) Electrophysiology of the paralemniscal-facial pathway. Soc Neurosci Abstr 11: 82

    Google Scholar 

  • McMahon SB, Wall PD (1985) Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res 333: 19–26

    Google Scholar 

  • Mesulam M-M (1982) Principles of horseradish peroxidase neurohistochemistry 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, Chichester, pp 1–151

    Google Scholar 

  • Munoz DP, Guitton D (1985) Tectospinal neurons in the cat have discharges coding gaze position error. Brain Res 341: 184–188

    Google Scholar 

  • Munoz DP, Guitton D (1986) Presaccadic burst discharges of tecto-reticulo-spinal neurons in the alert head-free and-fixed cat. Brain Res 398: 185–190

    Google Scholar 

  • Olucha F, Martínez-García F, López-Garcia C (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J Neurosci Meth 13: 131–138

    Google Scholar 

  • Papez JW, Freeman GL (1930) Superior colliculi and their fibre connections in the rat. J Comp Neurol 51: 409–439

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, Sydney

    Google Scholar 

  • Peterson BW, Fukushima K (1982) The reticulospinal system and its role in generating vestibular and visuomotor reflexes. In: Sjölund B, Björklund A (eds) Brain stem control of spinal reflexes. Elsevier, Amsterdam, pp 225–251

    Google Scholar 

  • Petrovický P (1976) Projections from the tectum mesencephali to the brain stem structures in the rat. Folia Morphol 24: 41–48

    Google Scholar 

  • Redgrave P, Mitchell IJ, Dean P (1987a) Descending projections from the superior colliculus in rat: a study using orthograde transport of wheatgerm-agglutinin conjugated horseradish peroxidase. Exp Brain Res 68: 147–167

    Google Scholar 

  • Redgrave P, Mitchell IJ, Dean P (1987b) Further evidence for segregated output channels from superior colliculus in rat: ipsilateral tecto-pontine and tecto-cuneiform projections have different cells of origin. Brain Res 413: 170–174

    Google Scholar 

  • Redgrave P, Odekunle A, Dean P (1986) Tectal cells of origin of predorsal bundle cells in rat: location and segregation from ipsilateral descending pathway. Exp Brain Res 63: 279–293

    Google Scholar 

  • Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 250: 482–524

    Google Scholar 

  • Sahibzada N, Dean P, Redgrave P (1986) Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6: 723–733

    Google Scholar 

  • Schiller PH (1985) The superior colliculus and visual function. In: Darien-Smith I (ed) Handbook of physiology — the nervous system, Vol 3. American Physiological Society, Bethesda, pp 457–505

    Google Scholar 

  • Skagerberg G, Björklund A, Lindvall O (1985) Further studies on the use of the fluorescent tracer true blue in combination with monoamine histochemistry. J Neurosci Meth 14: 25–40

    Google Scholar 

  • Swanson LW, Mogenson GJ, Gerfen CR, Robinson P (1984) Evidence for a projection from the lateral preoptic area and substantia innominata to the ‘mesencephalic locomotor region’ in the rat. Brain Res 295: 161–178

    Google Scholar 

  • Tehovnik EJ, Yeomans JS (1986) Two converging brainstem pathways mediating circling behavior. Brain Res 385: 329–342

    Google Scholar 

  • Tokunaga A, Otani K (1976) Dendritic patterns of neurons in the rat superior colliculus. Exp Neurol 52: 189–205

    Google Scholar 

  • Waldron HA, Gwyn DG (1969) Descending nerve tracts in the spinal cord of the rat. I. Fibres from the midbrain. J Comp Neurol 137: 143–154

    Google Scholar 

  • Wilson PM (1985) A photographic perspective on the origins, form, course and relations of the acetylcholinesterase-containing fibres of the dorsal tegmental pathway in the rat brain. Brain Res Rev 10: 85–118

    Google Scholar 

  • Wurtz RH, Albano JE (1980) Visual-motor function of the primate superior colliculus. Ann Rev Neurosci 3: 189–226

    Google Scholar 

  • Zemlan FP, Behbehani MM (1984) Afferent projections to the nucleus cuneiformis in the rat. Neurosci Lett 52: 103–109

    Google Scholar 

Download references

Author information

Author notes

  1. I. J. Mitchell

    Present address: Department of Cell and Structural Biology, Stopford Building, Oxford Road, M13 9PT, Manchester, UK

  2. A. Odekunle

    Present address: Department of Anatomy, College of Medical Sciences, University of Benin, P.M.B. 1154, Benin City, Nigeria

  3. A. Clark

    Present address: Psychological Laboratory, University of St. Andrews, KY169JU, St. Andrews, UK

Authors and Affiliations

  1. Department of Psychology, University of Sheffield, S10 2TN, Sheffield, UK

    P. Redgrave, P. Dean, I. J. Mitchell, A. Odekunle & A. Clark

Authors
  1. P. Redgrave
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Dean
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. J. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Odekunle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Redgrave, P., Dean, P., Mitchell, I.J. et al. The projection from superior colliculus to cuneiform area in the rat. Exp Brain Res 72, 611–625 (1988). https://doi.org/10.1007/BF00250606

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00250606

Key words

Search

Navigation