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

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Abstract

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.

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Fig. 1A–E.
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Abbreviations

ABD:

abducens nucleus

Cb:

cerebellum

HL:

hypothalamic lobe

IRRF:

inferior rhombencephalic reticular formation

IS:

injection site

MRF:

mesencephalic reticular formation

MRRF:

medial rhombencephalic reticular formation

nMLF:

nucleus of the medial longitudinal fasciculus

OCM:

oculomotor nucleus

OT:

optic tectum

SRRF:

superior rhombencephalic reticular formation

Tel:

telencephalon

TS:

torus semicircularis

VCb:

cerebellar valve

VL:

vagal lobe

References

  • 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 84:1035–1049

    PubMed  Google Scholar 

  • Appell PP, Behan M (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol 302:143–158

    CAS  PubMed  Google Scholar 

  • Brandt HM, Apkarian AV (1992) Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Methods 45:35–40

    CAS  PubMed  Google Scholar 

  • 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 151:31–47

    PubMed  Google Scholar 

  • 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 413:55–67

    Article  PubMed  Google Scholar 

  • Chen B, May PJ (2000) The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration. Exp Brain Res 131:10–21

    CAS  PubMed  Google Scholar 

  • 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 57:167–174

    CAS  PubMed  Google Scholar 

  • Cohen B, Matsuo V, Fradin J, Raphan T (1985) Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Exp Brain Res 57:605–616

    CAS  PubMed  Google Scholar 

  • 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 12:486–502

    CAS  PubMed  Google Scholar 

  • 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 114:461–471

    CAS  PubMed  Google Scholar 

  • 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 319:539–559

    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 tecto-reticulo-spinal pathway. Neuroscience 19:367–380

    Article  CAS  PubMed  Google Scholar 

  • Demski LS (1982) Eye movements and related behavioral responses evoked by electrical stimulation of the brain in free-swimming sunfish. Brain Behav Evol 20:182–195

    CAS  PubMed  Google Scholar 

  • 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 317–359

  • Demski LS, Bauer DH (1975) Eye movements evoked by electrical stimulation of the brain in anesthetized fishes. Brain Behav Evol 11:109–129

    CAS  PubMed  Google Scholar 

  • 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 404:473–488

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309–329

    Google Scholar 

  • 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 64:421–433

    CAS  PubMed  Google Scholar 

  • Fiebig E, Ebbesson SOE, Meyer DL (1983) Afferent connections of the optic tectum in the piranha (Serrasalmus nattereri). Cell Tissue Res 231:55–72

    CAS  PubMed  Google Scholar 

  • 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 40:573–588

    PubMed  Google Scholar 

  • 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 46:243–256

    CAS  PubMed  Google Scholar 

  • Grantyn AA, Dalezios Y, Kitama T, Moschovakis AK (1997) An anatomical basis for the spatio-temporal transformation in the saccadic system. Soc Neurosci Abstr 23:1295

    Google Scholar 

  • 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 451:346–361

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 146:205–220

    Article  CAS  PubMed  Google Scholar 

  • Grover BG, Sharma SC (1979) Tectal projections in the goldfish (Carassius auratus): a degeneration study. J Comp Neurol 184:435–454

    CAS  PubMed  Google Scholar 

  • Grover BG, Sharma SC (1981) Organization of extrinsic tectal connections in goldfish (Carassius auratus). J Comp Neurol 196:471–488

    CAS  PubMed  Google Scholar 

  • 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 39:63–73

    CAS  PubMed  Google Scholar 

  • Handel A, Glimcher PW (1997) Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. J Neurophysiol 78:2164–2175

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • 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 401:411–428

    Article  CAS  PubMed  Google Scholar 

  • 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 120:291–305

    Article  CAS  PubMed  Google Scholar 

  • Herrero L, Pérez P, Núñez-Abades P, Hardy O, Torres B (1999) Tectotectal connectivity in goldfish. J Comp Neurol 411:455–471

    Article  CAS  PubMed  Google Scholar 

  • Hofmann MH, Ebbesson SOE, Meyer DL (1990) Tectal afferents in Rana pipiens. A reassessment questioning the comparability of HRP results. J Hirnforsch 31:337–340

    CAS  PubMed  Google Scholar 

  • 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 687–773

  • Jiang ZD, Moore DR, King AJ (1997) Sources of subcortical projections to the superior colliculus in the ferret. Brain Res 755:279–292

    Article  CAS  PubMed  Google Scholar 

  • 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 39:87–96

    PubMed  Google Scholar 

  • Kunzle H (1997) Connections of the superior colliculus with the tegmentum and the cerebellum in the hedgehog tenrec. Neurosci Res 28:127–145

    Article  CAS  PubMed  Google Scholar 

  • 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 564:1–11

    CAS  PubMed  Google Scholar 

  • Langer TP, Kaneko CR (1984) Brainstem afferents to the omnipause region in the cat: a horseradish peroxidase study. J Comp Neurol 230:444–458

    Google Scholar 

  • Langer TP, Kaneko CR (1990) Brainstem afferents to the oculomotor omnipause neurons in monkey. J Comp Neurol 295:413–427

    CAS  PubMed  Google Scholar 

  • 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 39:163–174

    Article  CAS  PubMed  Google Scholar 

  • Luiten PGM (1981) Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Res 220:51–65

    Article  CAS  PubMed  Google Scholar 

  • 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 291:103–127

    CAS  PubMed  Google Scholar 

  • 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 92:194–208

    CAS  PubMed  Google Scholar 

  • Masino T, Knudsen EI (1993) Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. J Neurosci 13:351–370

    CAS  PubMed  Google Scholar 

  • 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 56:405–408

    Google Scholar 

  • Moschovakis AK, Highstein SM (1994) The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 17:465–488

    CAS  PubMed  Google Scholar 

  • Moschovakis AK, Scudder CA, Highstein SM (1991a) Structure of the primate oculomotor generator. I. Medium-lead burst neurons with upward on-directions. J Neurophysiol 65:203–217

    CAS  PubMed  Google Scholar 

  • 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 65:218–229

    CAS  PubMed  Google Scholar 

  • Moschovakis AK, Kitama T, Dalezios Y, Petit J, Brandi AM, Grantyn AA (1998) An anatomical substrate for the spatiotemporal transformation. J Neurosci 18:10219–10229

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Northmore DPM, Levine ES, Scheneider GE (1988) Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595–605

    CAS  PubMed  Google Scholar 

  • 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 91:807–811

    CAS  PubMed  Google Scholar 

  • 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 427:405–416

    Article  PubMed  Google Scholar 

  • 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 413:170–174

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 337–374

  • 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 178:293–305

    Google Scholar 

  • 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 3:131–134

    CAS  PubMed  Google Scholar 

  • Salas C, Herrero L, Rodríguez F, Torres B (1997) Tectal codification of eye movements in goldfish studied by electrical microstimulation. Neuroscience 78:271–288

    Article  CAS  PubMed  Google Scholar 

  • Schlussman SD, Kobylack MA, Dunn-Meynell AA, Sharma SC (1990) Afferent connections of the optic tectum in channel catfish Ictalurus punctatus. Cell Tissue Res 262:531–541

    CAS  PubMed  Google Scholar 

  • Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements. A modern synthesis. Exp Brain Res 142:439–462

    Article  PubMed  Google Scholar 

  • Sereno MI (1985) Tectoreticular pathways in the turtle, Pseudemys scripta. I: Morphology of tectoreticular axons. J Comp Neurol 233:48–90

    CAS  PubMed  Google Scholar 

  • Smeets WJAJ (1981) Efferent tectal pathways in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 19:513–523

    Google Scholar 

  • Soetedjo R, Kaneko CS, Fuchs AF (2002) Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J Neurophysiol 87:679–695

    PubMed  Google Scholar 

  • Sparks DL, Mays LE (1990) Signal transformation required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336

    CAS  PubMed  Google Scholar 

  • 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 56:85–98

    Google Scholar 

  • 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 1315–1524

  • 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 57:345–348

    Article  CAS  PubMed  Google Scholar 

  • Uetmasu K, Todo T (1997) Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp, Cyprinus carpio. Brain Res 773:1–7

    Article  PubMed  Google Scholar 

  • Vanegas H (1984) Comparative neurology of the optic tectum. Plenum, New York

  • Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Methods 41:239–254

    CAS  PubMed  Google Scholar 

  • 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 60:769–797

    CAS  PubMed  Google Scholar 

  • Waitzman DM, Ma TP, Optican LM, Wurtz RH (1991) Superior colliculus neurons mediate the dynamic characteristics of saccades. J Neurophysiol 66:1716–1737

    CAS  PubMed  Google Scholar 

  • Waitzman DM, Silakov VL, Cohen B (1996) Central mesencephalic reticular formation (cMRF) neurons discharging before and during eye movements. J Neurophysiol 75:1546–1572

    CAS  PubMed  Google Scholar 

  • 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 83:2260–2284

    CAS  PubMed  Google Scholar 

  • 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 83:2285–2299

    CAS  PubMed  Google Scholar 

  • 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 956:111–129

    PubMed  Google Scholar 

  • Wilczyniski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: an HRP study. J Comp Neurol 173:219–230

    PubMed  Google Scholar 

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Acknowledgements.

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

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Correspondence to B. Torres.

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This work is dedicated to the memory of Dr. Olivier Hardy, who recently passed away. He devoted years of effort with us in previous studies aimed at elucidating the neural substratum underlying decodification of the tectal signal in goldfish. We are indebted to him for many years of friendship.

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Pérez-Pérez, M.P., Luque, M.A., Herrero, L. et al. Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation. Exp Brain Res 151, 123–135 (2003). https://doi.org/10.1007/s00221-003-1432-6

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