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Synaptic circuitry in the retinorecipient layers of the optic tectum of the lamprey (Lampetra fluviatilis). A combined hodological, GABA and glutamate immunocytochemical study

Brain Structure and Function volume 213, Article number: 395 (2009) Cite this article

Abstract

The ultrastructure of the retinorecipient layers of the lamprey optic tectum was analysed using tract tracing techniques combined with GABA and glutamate immunocytochemistry. Two types of neurons were identified; a population of large GABA-immunonegative cells, and a population of smaller, highly GABA-immunoreactive interneurons, some of whose dendrites contain synaptic vesicles (DCSV). Five types of axon terminals were identified and divided into two major categories. The first of these are GABA-immunonegative, highly glutamate-immunoreactive, contain round synaptic vesicles, make asymmetrical synaptic contacts, and can in turn be divided into AT1 and AT2 terminals. The AT1 terminals are those of the retinotectal projection. The origin of the nonretinal AT2 terminals could not be determined. AT1 and AT2 terminals establish synaptic contacts with DCSV, with dendrites of the retinopetal neurons (DRN), and with conventional dendritic (D) profiles. The terminals of the second category are GABA-immunoreactive and can similarly be divided into AT3 and AT4 terminals. The AT3 terminals contain pleiomorphic synaptic vesicles and make symmetrical synaptic contacts for the most part with glutamate-immunoreactive D profiles. The AT4 terminals contain rounded synaptic vesicles and make asymmetrical synaptic contacts with DRN, with DCSV, and with D profiles. A fifth, rarely observed category of terminals (AT5) contain both clear synaptic vesicles and a large number of dense-core vesicles. Synaptic triads involving AT1, AT2 or AT4 terminals are rare. Our findings are compared to these of previous studies of the fine structure and immunochemical properties of the retinorecipient layers of the optic tectum or superior colliculus of Gnathostomes.

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Abbreviations

AOA:

Area optica accessoria

AT1:

Type 1 axon terminals

AT2:

Type 2 axon terminals

AT3:

Type 3 axon terminals

AT4:

Type 4 axon terminals

AT5:

Type 5 axon terminals

AX2:

Axon of type 2 terminal

AXg:

GABA-immunoreactive axon

BA:

Background immunolabelling

CGL:

Corpus geniculatum laterale

CH:

Cerebral hemisphere

CV:

Centrifugal visual pathway

D:

Conventional dendrite

DCSV:

Dendrite of interneuron containing synaptic vesicles

DCSV1:

Dendrite of interneuron containing synaptic vesicles of the first type

DCSV2:

Dendrite of interneuron containing synaptic vesicles of the second type

Dg+:

Conventional GABA-immunoreactive dendrite of interneuron

Dg−:

Conventional GABA-immunonegative dendrite of efferent neuron

DG+:

Conventional glutamate-immunoreactive dendrite of efferent neuron

DG−:

Conventional glutamate-immunonegative dendrite of interneuron

DRN:

HRP-labelled dendrite of the centrifugal neurons of RMA

DRNg+:

HRP-labelled GABA-immunoreactive dendrite of the centrifugal neurons of RMA

GABA:

γ-Aminobutyric acid

HI:

Horizontal interneurons

HRP:

Horseradish peroxidase

HY:

Hypothalamus

INS:

Soma of interneuron

ir:

Immunoreactive

M5:

Centrifugal visual neurons of the nucleus M5 of Schober

MT:

Mesencephalic tegmentum

NP:

Nucleus preopticus

NPO:

Nucleus of the postoptic commissure

NPR:

Nucleus pretectalis

OB:

Olfactory bulb

OC:

Optic chiasma

OF:

Optic fibre

ON:

Optic nerve

PCSV:

Profiles containing synaptic vesicles

PNS:

Soma of projecting neuron

RI:

Radial interneurons

RITC:

Rhodamine β-isothiocyanate

RMA:

Centrifugal visual neurons of the reticular mesencephalic area

RP:

Retinal projections

TO:

Tectum opticum

SCE:

Stratum cellulare ependimale

SCFC:

Stratum cellulare et fibrosum centrale

SCFE:

Stratum cellulare et fibrosum externum

SCFI:

Stratum cellulare et fibrosum internum

SCP:

Stratum cellulare periventriculare

SFP:

Stratum fibrosum periventriculare

SM:

Stratum marginale

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Acknowledgments

We thank Denis LeCren for his extremely skilful photographic assistance. This work was supported by MNHN, CNRS (France), Academy of Sciences (Russia) NSERC (Canada).

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Affiliations

  1. Département Régulations, Développement et Diversité Moléculaire, USM 501, CNRS UMR 7221, Muséum National d’Histoire Naturelle, Paris, France

    Jacques Repérant, Roger Ward, Monique Médina, Natalia B. Kenigfest, Dom Miceli & Bruno Jay

  2. Laboratoire de Neuropsychologie Expérimentale et Comparée, Université du Québec, Trois-Rivières, Canada

    Jacques Repérant, Roger Ward, Monique Médina & Dom Miceli

  3. Laboratory of Evolution of Neuronal Interactions, Sechenov Institute, Russian Academy of Sciences, St. Petersburg, Russia

    Natalia B. Kenigfest

  4. INSERM U-616, Hôpital de la Salpêtrière, Paris, France

    Jean-Paul Rio

  5. Département RDDM, USM 501, CNRS UMR 7221, Muséum National d’Histoire Naturelle, CP 55, Bâtiment d’Anatomie Comparée, 57 rue Cuvier, 75231, Paris Cedex 05, France

    Monique Médina

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  1. Jacques Repérant
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  2. Roger Ward
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  3. Monique Médina
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  4. Natalia B. Kenigfest
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  5. Jean-Paul Rio
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  6. Dom Miceli
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  7. Bruno Jay
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Correspondence to Monique Médina.

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Repérant, J., Ward, R., Médina, M. et al. Synaptic circuitry in the retinorecipient layers of the optic tectum of the lamprey (Lampetra fluviatilis). A combined hodological, GABA and glutamate immunocytochemical study. Brain Struct Funct 213, 395 (2009). https://doi.org/10.1007/s00429-009-0205-9

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Keywords

  • Lamprey
  • Optic tectum
  • Synaptic connections
  • Immunocytochemistry