Experimental Brain Research

, Volume 151, Issue 1, pp 123–135 | Cite as

Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation

  • M. P. Pérez-Pérez
  • M. A. Luque
  • L. Herrero
  • P. A. Nunez-Abades
  • B. TorresEmail author
Research Article


The optic tectum of goldfish, as in other vertebrates, plays a major role in the generation of orienting movements, including eye saccades. To perform these movements, the optic tectum sends a motor command through the mesencephalic and rhombencephalic reticular formation, to the extraocular motoneurons. Furthermore, the tectal command is adjusted by a feedback signal arising from the reticular targets. Since the features of the motor command change with respect to the tectal site, the present work was devoted to determining, quantitatively, the particular reciprocal connectivity between the reticular regions and tectal sites having different motor properties. With this aim, the bidirectional tracer, biotin dextran amine, was injected into anteromedial tectal sites, where eye movements with small horizontal and large vertical components were evoked, or into posteromedial tectal sites, where eye movements with large horizontal and small vertical components were evoked. Labeled boutons and somas were then located and counted in the reticular formation. Both were more numerous in the mesencephalon than in the rhombencephalon, and ipsilaterally than contralaterally, with respect to the injection site. Furthermore, the somas showed a tendency to be located in the area containing the most dense labeling of synaptic endings. In addition, labeled boutons were often observed in close association with retrogradely stained neurons, suggesting the presence of a tectoreticular feedback circuit. Following the injection in the anteromedial tectum, most of the boutons and labeled neurons were found in the reticular formation rostral to the oculomotor nucleus. Conversely, following the injection in the posteromedial tectum, most of the boutons and neurons were also located in the caudal mesencephalic reticular formation. Finally, boutons and neurons were found in the rhombencephalic reticular formation surrounding the abducens nucleus. They were more numerous following the injection in the posteromedial tectum. These results demonstrate characteristic patterns of reciprocal connectivity between physiologically different tectal sites and the mesencephalic and rhombencephalic reticular formation. These patterns are discussed in the framework of the neural substratum that underlies the codification of orienting movements in goldfish.


Optic tectum Tectoreticular pathways Saccadic system Orienting eye movements Teleost 



abducens nucleus




hypothalamic lobe


inferior rhombencephalic reticular formation


injection site


mesencephalic reticular formation


medial rhombencephalic reticular formation


nucleus of the medial longitudinal fasciculus


oculomotor nucleus


optic tectum


superior rhombencephalic reticular formation




torus semicircularis


cerebellar valve


vagal lobe



The work was supported by a grant (BFI2000-0335) from the Spanish Ministerio de Ciencia y Tecnología.


  1. Akasay E, Baker R, Seung HS, Tank DW (2000) Anatomy and discharge properties of pre-motor neurons in the goldfish medulla that have eye-position signals during fixations. J Neurophysiol 84:1035–1049PubMedGoogle Scholar
  2. Appell PP, Behan M (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol 302:143–158PubMedGoogle Scholar
  3. Brandt HM, Apkarian AV (1992) Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Methods 45:35–40PubMedGoogle Scholar
  4. Büttner-Ennever JA, Büttner U (1978) A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151:31–47PubMedGoogle Scholar
  5. Büttner-Ennever JA, Horn AK, Henn V, Cohen B (1999) Projections from the superior colliculus motor map to omnipause neurons in monkey. J Comp Neurol 413:55–67CrossRefPubMedGoogle Scholar
  6. Chen B, May PJ (2000) The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration. Exp Brain Res 131:10–21PubMedGoogle Scholar
  7. Cohen B, Büttner-Ennever JA (1984) Projections from the superior colliculus to a region of the central mesencephalic reticular formation (cMRF) associated with horizontal saccadic eye movements. Exp Brain Res 57:167–174PubMedGoogle Scholar
  8. Cohen B, Matsuo V, Fradin J, Raphan T (1985) Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Exp Brain Res 57:605–616PubMedGoogle Scholar
  9. Corvisier J, Hardy O (1991) Possible excitatory and inhibitory feedback to the superior colliculus: a combined retrograde and immunocytochemical study in the prepositus hypoglossi nucleus of the guinea pig. Neurosci Res 12:486–502PubMedGoogle Scholar
  10. Corvisier J, Hardy O (1997) Topographical characteristics of preposito-collicular projections in the cat as revealed by Phaseolus vulgaris-leucoagglutinin technique. A possible organization underlying temporal-to-spatial transformations. Exp Brain Res 114:461–471PubMedGoogle Scholar
  11. Cowie RJ, Holstege G (1992) Dorsal mesencephalic projections to the pons, medulla and spinal cord in the cat: limbic and non-limbic components. J Comp Neurol 319:539–559Google Scholar
  12. 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 tecto-reticulo-spinal pathway. Neuroscience 19:367–380CrossRefPubMedGoogle Scholar
  13. Demski LS (1982) Eye movements and related behavioral responses evoked by electrical stimulation of the brain in free-swimming sunfish. Brain Behav Evol 20:182–195PubMedGoogle Scholar
  14. Demski LS (1983) Behavioral effects of electrical stimulation of the brain. In: Davis RE, Northcutt RG (eds) Fish neurobiology, vol. 2. Higher brain areas and functions. University of Michigan Press, Ann Arbor, pp 317–359Google Scholar
  15. Demski LS, Bauer DH (1975) Eye movements evoked by electrical stimulation of the brain in anesthetized fishes. Brain Behav Evol 11:109–129PubMedGoogle Scholar
  16. Dicke U (1999) Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. I: Tracer study of projection neurons and their pathways. J Comp Neurol 404:473–488CrossRefPubMedGoogle Scholar
  17. Ebbesson SOE, Vanegas H (1976) Projections of the optic tectum in two teleost species. J Comp Neurol 165:161–180PubMedGoogle Scholar
  18. Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309–329Google Scholar
  19. Ellard CG, Goodale MA (1986) The role of the predorsal bundle in head and body movements elicited by electrical stimulation of the superior colliculus in the Mongolian gerbil. Exp Brain Res 64:421–433PubMedGoogle Scholar
  20. Fiebig E, Ebbesson SOE, Meyer DL (1983) Afferent connections of the optic tectum in the piranha (Serrasalmus nattereri). Cell Tissue Res 231:55–72PubMedGoogle Scholar
  21. Gestring P, Sterling P (1977) Anatomy and physiology of goldfish oculomotor system. II. Firing patterns of neurons in abducens nucleus and surrounding medulla and their relation to eye movements. J Neurophysiol 40:573–588PubMedGoogle Scholar
  22. Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbospinal tract. Exp Brain Res 46:243–256PubMedGoogle Scholar
  23. Grantyn AA, Dalezios Y, Kitama T, Moschovakis AK (1997) An anatomical basis for the spatio-temporal transformation in the saccadic system. Soc Neurosci Abstr 23:1295Google Scholar
  24. Grantyn A, Brandi AM, Dubayle D, Graf W, Ugolini G, Hadjidimitrakis K, Moschovakis A (2002) Density gradients of trans-synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey. J Comp Neurol 451:346–361CrossRefPubMedGoogle Scholar
  25. Grobstein P (1988) Between the retinotectal projection and directed movement: topography of a sensorimotor interface. Brain Behav Evol 31:34–48PubMedGoogle Scholar
  26. Grofova O, Ottersen OP, Rinvik E (1978) Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Res 146:205–220CrossRefPubMedGoogle Scholar
  27. Grover BG, Sharma SC (1979) Tectal projections in the goldfish (Carassius auratus): a degeneration study. J Comp Neurol 184:435–454PubMedGoogle Scholar
  28. Grover BG, Sharma SC (1981) Organization of extrinsic tectal connections in goldfish (Carassius auratus). J Comp Neurol 196:471–488PubMedGoogle Scholar
  29. 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 39:63–73PubMedGoogle Scholar
  30. Handel A, Glimcher PW (1997) Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. J Neurophysiol 78:2164–2175PubMedGoogle Scholar
  31. Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173:583–612PubMedGoogle Scholar
  32. Herrero L, Corvisier J, Hardy O, Torres B (1998a) Influence of the tectal zone on the distribution of synaptic boutons in the brainstem of goldfish. J Comp Neurol 401:411–428CrossRefPubMedGoogle Scholar
  33. Herrero L, Rodríguez F, Salas C, Torres B (1998b) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120:291–305CrossRefPubMedGoogle Scholar
  34. Herrero L, Pérez P, Núñez-Abades P, Hardy O, Torres B (1999) Tectotectal connectivity in goldfish. J Comp Neurol 411:455–471CrossRefPubMedGoogle Scholar
  35. Hofmann MH, Ebbesson SOE, Meyer DL (1990) Tectal afferents in Rana pipiens. A reassessment questioning the comparability of HRP results. J Hirnforsch 31:337–340PubMedGoogle Scholar
  36. Huerta MF, Harting JK (1984) The mammalian superior colliculus: studies of its morphology and connections. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum, New York, pp 687–773Google Scholar
  37. Jiang ZD, Moore DR, King AJ (1997) Sources of subcortical projections to the superior colliculus in the ferret. Brain Res 755:279–292CrossRefPubMedGoogle Scholar
  38. Jurgens R, Becker W, Kornhuber HH (1981) Natural and drug-induced variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biol Cybern 39:87–96PubMedGoogle Scholar
  39. Kunzle H (1997) Connections of the superior colliculus with the tegmentum and the cerebellum in the hedgehog tenrec. Neurosci Res 28:127–145CrossRefPubMedGoogle Scholar
  40. Lachica EA, Mavity-Hudson JA, Casagrande VA (1991) Morphological details of primate axons and dendrites revealed by extracellular injections of biocytin: an economic and reliable alternative to PHA-L. Brain Res 564:1–11PubMedGoogle Scholar
  41. Langer TP, Kaneko CR (1984) Brainstem afferents to the omnipause region in the cat: a horseradish peroxidase study. J Comp Neurol 230:444–458Google Scholar
  42. Langer TP, Kaneko CR (1990) Brainstem afferents to the oculomotor omnipause neurons in monkey. J Comp Neurol 295:413–427PubMedGoogle Scholar
  43. Lapper SP, Bolam JP (1991) The anterograde and retrograde transport of neurobiotin in the central nervous system of the rat: comparison with biocytin. J Neurosci Methods 39:163–174CrossRefPubMedGoogle Scholar
  44. Luiten PGM (1981) Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Res 220:51–65CrossRefPubMedGoogle Scholar
  45. Masino T, Grobstein P (1990) Tectal connectivity in the frog Rana pipiens. II. Tectotegmental projections and a general analysis of topographic organization. J Comp Neurol 291:103–127PubMedGoogle Scholar
  46. Masino T, Knudsen EI (1992) Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Exp Brain Res 92:194–208PubMedGoogle Scholar
  47. Masino T, Knudsen EI (1993) Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. J Neurosci 13:351–370PubMedGoogle Scholar
  48. May PJ, Warren S, Chen B, Richmond FJR, Olivier E (2002) Midbrain reticular formation circuitry subserving gaze in the cat. Ann N Y Acad Sci 56:405–408Google Scholar
  49. Moschovakis AK, Highstein SM (1994) The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 17:465–488PubMedGoogle Scholar
  50. Moschovakis AK, Scudder CA, Highstein SM (1991a) Structure of the primate oculomotor generator. I. Medium-lead burst neurons with upward on-directions. J Neurophysiol 65:203–217PubMedGoogle Scholar
  51. Moschovakis AK, Scudder CA, Highstein SM, Warren JD (1991b) Structure of the primate oculomotor generator. II. Medium-lead burst neurons with downward on-directions. J Neurophysiol 65:218–229PubMedGoogle Scholar
  52. Moschovakis AK, Kitama T, Dalezios Y, Petit J, Brandi AM, Grantyn AA (1998) An anatomical substrate for the spatiotemporal transformation. J Neurosci 18:10219–10229PubMedGoogle Scholar
  53. Northcutt RG, Butler AB (1980) Projections of the optic tectum in the longnose gar, Lepisosteus osseus. Brain Res 190:333–346CrossRefPubMedGoogle Scholar
  54. Northmore DPM, Levine ES, Scheneider GE (1988) Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595–605PubMedGoogle Scholar
  55. Pastor AM, De la Cruz RR, Baker R (1994) Eye position and eye velocity integrators reside in separate brainstem nuclei. Proc Natl Acad Sci U S A 91:807–811PubMedGoogle Scholar
  56. Pérez-Pérez MP, Herrero L, Torres B (2000) Connectivity of the tectal zones coding for upward and downward oblique eye movements in goldfish. J Comp Neurol 427:405–416CrossRefPubMedGoogle Scholar
  57. Redgrave P, Mitchell IJ, Dean P (1987) Descending projections from the superior colliculus in rat: ipsilateral tecto-pontine and tecto-cuneiform projections have different cells of origin. Brain Res 413:170–174CrossRefPubMedGoogle Scholar
  58. Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808PubMedGoogle Scholar
  59. Robinson DA (1975) Oculomotor control signals. In: Bach-y-Rita P, Lennerstrand G (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon, Oxford, pp 337–374Google Scholar
  60. Roche King J, Comer CM (1996) Visually elicited turning behavior in Rana pipiens: comparative organization and neural control of escape and prey capture. J Comp Neurol 178:293–305Google Scholar
  61. Salas C, Navarro F, Torres B, Delgado-García JM (1992) Effects of diazepam and d-amphetamine on rhythmic pattern of eye movements in goldfish. Neuroreport 3:131–134PubMedGoogle Scholar
  62. Salas C, Herrero L, Rodríguez F, Torres B (1997) Tectal codification of eye movements in goldfish studied by electrical microstimulation. Neuroscience 78:271–288CrossRefPubMedGoogle Scholar
  63. Schlussman SD, Kobylack MA, Dunn-Meynell AA, Sharma SC (1990) Afferent connections of the optic tectum in channel catfish Ictalurus punctatus. Cell Tissue Res 262:531–541PubMedGoogle Scholar
  64. Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements. A modern synthesis. Exp Brain Res 142:439–462CrossRefPubMedGoogle Scholar
  65. Sereno MI (1985) Tectoreticular pathways in the turtle, Pseudemys scripta. I: Morphology of tectoreticular axons. J Comp Neurol 233:48–90PubMedGoogle Scholar
  66. Smeets WJAJ (1981) Efferent tectal pathways in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 19:513–523Google Scholar
  67. Soetedjo R, Kaneko CS, Fuchs AF (2002) Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J Neurophysiol 87:679–695PubMedGoogle Scholar
  68. Sparks DL, Mays LE (1990) Signal transformation required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336PubMedGoogle Scholar
  69. Sparks DL, Barton EJ, Gandhi NJ, Nelson J (2002) Studies of the role of the paramedian pontine reticular formation in the control of head-restrained and head-unrestrained gaze shifts. Ann N Y Acad Sci 56:85–98Google Scholar
  70. Ten Donkelaar HJ (1998) Reptiles. In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrales, vol 2. Springer, Berlin Heidelberg New York, pp 1315–1524Google Scholar
  71. Torres B, Pérez-Pérez MP, Herrero L, Ligero M, Nunez-Abades PA (2002) Neural substrata underlying tectal eye movement codification in goldfish. Brain Res Bull 57:345–348CrossRefPubMedGoogle Scholar
  72. Uetmasu K, Todo T (1997) Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp, Cyprinus carpio. Brain Res 773:1–7CrossRefPubMedGoogle Scholar
  73. Vanegas H (1984) Comparative neurology of the optic tectum. Plenum, New YorkGoogle Scholar
  74. Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Methods 41:239–254PubMedGoogle Scholar
  75. Vidal PP, May PJ, Baker R (1988) Synaptic organization of the tectal-facial pathways in the cat. I. Synaptic potential following collicular stimulation. J Neurophysiol 60:769–797PubMedGoogle Scholar
  76. Waitzman DM, Ma TP, Optican LM, Wurtz RH (1991) Superior colliculus neurons mediate the dynamic characteristics of saccades. J Neurophysiol 66:1716–1737PubMedGoogle Scholar
  77. Waitzman DM, Silakov VL, Cohen B (1996) Central mesencephalic reticular formation (cMRF) neurons discharging before and during eye movements. J Neurophysiol 75:1546–1572PubMedGoogle Scholar
  78. Waitzman DM, Silakov VL, DePalma-Bowles S, Ayers AS (2000a) Effects of reversible inactivation of the primate mesencephalic reticular formation. I. Hypermetric goal-directed saccades. J Neurophysiol 83:2260–2284PubMedGoogle Scholar
  79. Waitzman DM, Silakov VL, DePalma-Bowles S, Ayers AS (2000b) Effects of reversible inactivation of the primate mesencephalic reticular formation. II. Hypometric vertical saccades. J Neurophysiol 83:2285–2299PubMedGoogle Scholar
  80. Waitzman DM, Pathmanathan J, Presnell R, Ayers A, DePalma S (2002) Contribution of the superior colliculus and the mesencephalic reticular formation to gaze control. Ann N Y Acad Sci 956:111–129PubMedGoogle Scholar
  81. Wilczyniski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: an HRP study. J Comp Neurol 173:219–230PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • M. P. Pérez-Pérez
    • 1
  • M. A. Luque
    • 1
  • L. Herrero
    • 1
  • P. A. Nunez-Abades
    • 1
  • B. Torres
    • 1
    • 2
    Email author
  1. 1.Lab. Neurobiologia de Vertebrados, Dept. Fisiologia y ZoologíaUniv. SevillaSevilleSpain
  2. 2.Dept. Fisiologia y Zoología, Fac. BiologiaUniv. SevillaSevilleSpain

Personalised recommendations