Skip to main content
Log in

Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Electrical stimulation of the optic tectum in many vertebrate species elicits eye, head or body orienting movements in the direction of the receptive field location recorded at the site of stimulation; in the barn owl, tectal stimulation produces short latency saccadic head movements (du Lac and Knudsen 1990). However, the barn owl, like other avians, lacks a direct projection from the tectum to the spinal cord, implying that less direct connections underlie tectally mediated head movements. In order to determine the pathways by which the tectum gains access to spinal cord circuitry, we searched for overlap regions between tectal efferent projections and the locations of cells afferent to the spinal cord. Tectal efferent pathways and terminal fields were revealed by anterograde labeling using horseradish peroxidase (HRP) or tritiated amino acids injected into the optic tectum. Cells afferent to the spinal cord were identified by means of retrograde labeling using HRP, rhodamine, or rhodamine-coupled latex beads injected into the cervical spinal cord. A comparison of results from the anterograde and retrograde labeling experiments demonstrated several areas of overlap. All of the cell groups that both received heavy tectal input and contained a high proportion of cells projecting to the spinal cord were located in the medial half of the midbrain and rhombencephalic tegmentum, and included the red nucleus, the interstitial nucleus of Cajal, the medial reticular formation, the nucleus reticularis pontis gigantocellularis, and the nucleus reticularis pontis oralis. All of these cell groups receive their tectal input from the medial efferent pathway, one of three major output pathways from the tectum. The other two output pathways (the rostral and the caudal) project to regions containing no more than a few scattered cells that are afferent to the spinal cord. Based on these data and on the functions of homologous cell groups in other vertebrates, we hypothesize that the medial efferent pathway and its brainstem target nuclei are primarily responsible for tectally mediated orienting head movements in the barn owl.

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

Access this article

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

  • Ariens-Kappers C, Huber GC, Crosby EC (1936) The comparative anatomy of the nervous system of vertebrates including man. Macmillan, New York

    Google Scholar 

  • Benowitz LI, Karten H (1976) Organization of tectofugal pathways in the pigeon: a retrograde transport study. J Comp Neurol 167:503–520

    Google Scholar 

  • Butler AB, Northcutt RG (1980) Projections of the optic tectum in the longnose gar, Lepisosteus osseus. Brain Res 190:333–346

    Google Scholar 

  • Büttner U, Büttner-Ennever JA, Henn V (1977) Vertical eye movement-related activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res 130:239–252

    Google Scholar 

  • Cabot JB, Reiner A, Bogan N (1982) Avian bulbospinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories, and laminar terminations. Prog Brain Res 57:79–107

    Google Scholar 

  • Craigie EH (1928) Observations on the brain of the humming bird (Chrysolampis mosquitus Linn and Chlorostilbon caribaeus Lawr) J Comp Neurol 45:377–481

    Google Scholar 

  • Dacey DM, Ulinski PS (1986) Optic tectum of the eastern garter snake, Thamnophis sirtalis. I. Efferent pathways. J Comp Neurol 245:1–28

    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 

  • Ebbesson SOE, Vanegas H (1976) Projections of the optic tectum in two teleost species. J Comp Neurol 165:161–180

    Google Scholar 

  • Fuchs AF, Kaneko CRS, Scudder CA (1985) Brainstem control of saccadic eye movements. Ann Rev Neurosci 8:307–338

    Google Scholar 

  • Grantyn A, Berthoz A (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Exp Brain Res66:339–354

    Google Scholar 

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

    Google Scholar 

  • Grantyn A, Grantyn R, Berthoz A, Ribas J (1982) Tectal control of vertical eye movements: a search for the underlying circuits in the mesecephalon. In: Roucoux A, Crommelinck M (eds): Physiological and pathological aspects of eye movements. Junk, The Hague, pp 337–344

    Google Scholar 

  • Graybiel AM (1978) A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers. Brain Res 145:365–374

    Google Scholar 

  • Grobstein P (1988) Between the retinotectal projection and directed movement: topography of a sensorimotor interface. Brain Behav Evol 31:34–48

    Google Scholar 

  • Grobstein P (1989) Organization in the sensorimotor interface: a case study with increased resolution. In: Ewert J-P, Arbib MA (eds) Visuomotor coordination: amphibians, comparisons, models and robots. Plenum, New York, 537–563

    Google Scholar 

  • Grobstein P (1990) Strategies for analyzing complex organization in the nervous system. I. Lesion experiments, the old rediscovered. In: E Schwartz (ed) Computational Neuroscience MIT Press, Cambridge, pp 245–255

    Google Scholar 

  • Grobstein P, Comer C (1983) The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog, Rana pipiens. J Comp Neurol 217:54–74

    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 

  • Hinsey JC, Ransom SW, Dixon HH (1930) Responses elicited by stimulation of the mesenephalic tegmentum in the cat. Arch Neurol Psychiat 24:966–977

    Google Scholar 

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

    Google Scholar 

  • Holstege G, Crowie RJ (1989) Projections from the rostral mesencephalic reticular formation to the spinal cord: an HRP and autoradiographic tracing study in the cat. Exp Brain Res 75:265–279

    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. Prog Brain Res 57:293–328

    Google Scholar 

  • Hunt SP, Kunzle H (1976) Observation on the projections and intrinsic organization of the pigeon optic tectum: an autoradiographic study based on anterograde and retrograde, axonal and dendritic flow. J Comp Neurol 170:153–172

    Google Scholar 

  • Ingram WR, Ransom SW, Hannet FI, Zeiss FR, Terwilliger EH (1932) Results of stimulation of the tegmentum with the Horsely-Clarke stereotaxic apparatus. Arch Neurol Psychiat 28:513–541

    Google Scholar 

  • Jungherr E (1945) Certain nuclear groups in the avian mesencephalon. J Comp Neurol 82:55–75

    Google Scholar 

  • Karten HJ, Hodos W (1967) A stereotaxic atlas of the brain of pigeon (Columbia livia). Johns Hopkins Press, Baltimore

    Google Scholar 

  • du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:136–146

    Google Scholar 

  • Lane JK (1978) A protocol for horseradish peroxidase histochemistry as practised in the lab of E. G. Jones In: Neuroanatomical techniques. (Society of Neuroscience Monograph)

  • Lawrence DG, Kuypers HG (1968) The functional organization of the motor system n the monkey. II. The effects of lesions of the descending brain-stem pathways. Brain 91:15–36

    CAS  PubMed  Google Scholar 

  • Masino T (1992) Brainstem control of orienting movements: Intrinsic coordinate systems and underlying circuitry. Brain Behav Evol 40:98–111

    Google Scholar 

  • Masino T, Knudsen EI (1990) Distinct neural circuits control horizontal and vertical components of head movement in the barn owl. Nature 345:434–437

    Google Scholar 

  • Masino T, Knudsen EI (1992) Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. J Neurosci (in press)

  • Masino T, Grobstein P (1989a) The organization of descending tectofugal pathways in frog, Rana pipiens. 1. Lateralization, parcellation and an intermediate spatial representation. Exp Brain Res 75:227–244

    Google Scholar 

  • Masino T, Grobstein P (1989b) The organization of the descending tectofugal pathways in the frog, Rana pipiens. 2. Evidence for the involvement of a tecto-tegmento-spinal pathway. Exp Brain Res 75:245–264

    Google Scholar 

  • Masino T, Grobstein P (1989c) Tectal connectivity in the frog, Rana pipiens: tectotegmental projections and a general analysis of topographic organization. J Comp Neurol 291:103–127

    Google Scholar 

  • Mesulum MM (1975) The blue reaction product in horseradish peroxidase neurohistochemistry: incubation parameters and visibility. J Histochem Cytochem 24:1273–1280

    Google Scholar 

  • Moschovakis AK, Karabalas AB (1985) Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP labelled efferent neurons located in the deepest layers of the superior colliculus of the cat. J Comp Neurol 239:276–308

    Google Scholar 

  • Ramon y Cajal S (1972) Histologie du system nerveaux de l'homme et des vertebrés, 2nd edn, vol II. Instituto Ramon y Cajal, Madrid, pp. 196–212

    Google Scholar 

  • Raphan T, Cohen B (1978) Brainstem mechanisms for rapid and slow eye movements. J Neurophysiol 34:920–936

    Google Scholar 

  • Reiner A, Karten HJ (1982) Laminar distribution of the cells of origin of the descending pathways in the pigeon (Columba livia). J Comp Neurol 201:165–187

    Google Scholar 

  • Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808

    Article  CAS  PubMed  Google Scholar 

  • Roucoux A, Guitton D, Crommelink M (1980) Stimulation of the superior colliculus in alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp Brain Res 39:75–85

    Google Scholar 

  • Takahashi TT, Konishi M (1988) Projections of nucleus angularis and nucleus laminaris to the lateral lemniscal nuclear complex of the barn owl. J Comp Neurol 274:212–238

    Google Scholar 

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

    Google Scholar 

  • Webster DMS, Steeves JD (1988) Origins of brainstem-spinal projection in the duck and goose. J Comp Neurol 273:573–583

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Masino, T., Knudsen, E.I. Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Exp Brain Res 92, 194–208 (1992). https://doi.org/10.1007/BF00227965

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227965

Key words

Navigation