Dual innervation of the lamprey retina by GABAergic and glutamatergic retinopetal fibers

Rio, J.P.; Repérant, J; Vesselkin, N. P.; Kenigfest-Rio, N.B; Miceli, D.

doi:10.1016/s0006-8993(02)03803-9

Cited by 10 publications

(8 citation statements)

References 33 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The retinopetal system of lampreys has been studied extensively (Vesselkin et al,1980,1984,1989,1996; De Miguel et al,1989; Rio et al,1993,2003; Rodicio et al,1995; Anadón et al,1998; Meléndez‐Ferro et al,2002a). Several immunocytochemical studies have revealed the presence of GABA in retinopetal cells of the midbrain and in fibers of the IPL, both in adult and in larval lampreys (Rio et al,1993; Vesselkin et al,1996; Anadón et al,1998; Meléndez‐Ferro et al,2002a).…”

Section: Discussionmentioning

confidence: 99%

“…Several immunocytochemical studies have revealed the presence of GABA in retinopetal cells of the midbrain and in fibers of the IPL, both in adult and in larval lampreys (Rio et al,1993; Vesselkin et al,1996; Anadón et al,1998; Meléndez‐Ferro et al,2002a). An experimental electron microscopic study in adult lamprey found that GABA‐ir fibers account for 45% of all tracer‐labeled retinopetal fibers but that GLU immunoreactivity is present in all retinopetal fibers (Rio et al,2003). The present results obtained with double‐immunofluorescence and spectral confocal microscopy in the larval retina confirm the presence of boutons of GABA‐ir retinopetal fibers in the larval IPL/optic fiber layer, where they appear to contact ganglion cell perikarya.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Presence of glutamate, glycine, and γ‐aminobutyric acid in the retina of the larval sea lamprey: Comparative immunohistochemical study of classical neurotransmitters in larval and postmetamorphic retinas

Villar-Cerviño

Abalo

Villar-Cheda

et al. 2006

J of Comparative Neurology

103

View full text Add to dashboard Cite

The neurochemistry of the retina of the larval and postmetamorphic sea lamprey was studied via immunocytochemistry using antibodies directed against the major candidate neurotransmitters [glutamate, glycine, gamma-aminobutyric acid (GABA), aspartate, dopamine, serotonin] and the neurotransmitter-synthesizing enzyme tyrosine hydroxylase. Immunoreactivity to rod opsin and calretinin was also used to distinguish some retinal cells. Two retinal regions are present in larvae: the central retina, with opsin-immunoreactive photoreceptors, and the lateral retina, which lacks photoreceptors and is mainly neuroblastic. We observed calretinin-immunostained ganglion cells in both retinal regions; immunolabeled bipolar cells were detected in the central retina only. Glutamate immunoreactivity was present in photoreceptors, ganglion cells, and bipolar cells. Faint to moderate glycine immunostaining was observed in photoreceptors and some cells of the ganglion cell/inner plexiform layer. No GABA-immunolabeled perikarya were observed. GABA-immunoreactive centrifugal fibers were present in the central and lateral retina. These centrifugal fibers contacted glutamate-immunostained ganglion cells. No aspartate, serotonin, dopamine, or TH immunoreactivity was observed in larvae, whereas these molecules, as well as GABA, glycine, and glutamate, were detected in neurons of the retina of recently transformed lamprey. Immunoreactivity to GABA was observed in outer horizontal cells, some bipolar cells, and numerous amacrine cells, whereas immunoreactivity to glycine was found in amacrine cells and interplexiform cells. Dopamine and serotonin immunoreactivity was found in scattered amacrine cells. Amacrine and horizontal cells did not express classical neurotransmitters (with the possible exception of glycine) during larval life, so transmitter-expressing cells of the larval retina appear to participate only in the vertical processing pathway.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Presence of glutamate, glycine, and γ‐aminobutyric acid in the retina of the larval sea lamprey: Comparative immunohistochemical study of classical neurotransmitters in larval and postmetamorphic retinas

Villar-Cerviño

Abalo

Villar-Cheda

et al. 2006

J of Comparative Neurology

103

View full text Add to dashboard Cite

show abstract

“…The other polyclonal glutamate antiserum (Sigma) was raised against a glutamate–glutaraldehyde–keyhole limpet hemocyanin (KLH) conjugate. The specificity of this glutamate antiserum was previously tested in lamprey neural tissue and homogenates, by methods including western blotting (for further details, see Vesselkin et al,1995; Rio et al,2003; Villar‐Cerviño et al,2006, 2011). The immunohistochemical results obtained with these polyclonal anti‐glutamate antibodies revealed the same pattern of glutamate‐ir cell populations in the brain and spinal cord.…”

Section: Methodsmentioning

confidence: 99%

Glutamatergic neuronal populations in the brainstem of the sea lamprey, Petromyzon marinus: An in situ hybridization and immunocytochemical study

Villar-Cerviño

Barreiro‐Iglesias

Fernández-López

et al. 2012

J of Comparative Neurology

View full text Add to dashboard Cite

Glutamate is the major excitatory neurotransmitter in vertebrates, and glutamatergic cells probably represent a majority of neurons in the brain. Physiological studies have demonstrated a wide presence of excitatory (glutamatergic) neurons in lampreys. The present in situ hybridization study with probes for the lamprey vesicular glutamate transporter (VGLUT) provides an anatomical basis for the general distribution and precise localization of glutamatergic neurons in the sea lamprey brainstem. Most glutamatergic neurons were found within the periventricular gray layer throughout the brainstem, with the following regions being of particular interest: the optic tectum, torus semicircularis, isthmus, dorsal and medial nuclei of the octavolateral area, dorsal column nucleus, solitary tract nucleus, motoneurons, and reticular formation. The reticular population revealed a high degree of cellular heterogeneity including small, medium-sized, large, and giant glutamatergic neurons. We also combined glutamate immunohistochemistry with neuronal tract-tracing methods or γ-aminobutyric acid (GABA) immunohistochemistry to better characterize the glutamatergic populations. Injection of Neurobiotin into the spinal cord revealed that retrogradely labeled small and medium-sized cells of some reticulospinal-projecting groups were often glutamate-immunoreactive, mostly in the hindbrain. In contrast, the large and giant glutamatergic reticulospinal perikarya mostly lacked glutamate immunoreactivity. These results indicate that glutamate immunoreactivity did not reveal the entire set of glutamatergic populations. Some spinal-projecting octaval populations lacked both VGLUT and glutamate. As regards GABA and glutamate, their distribution was largely complementary, but colocalization of glutamate and GABA was observed in some small neurons, suggesting that glutamate immunohistochemistry might also detect non-glutamatergic cells or neurons that co-release both GABA and glutamate.

show abstract

“…At least some of the retinotegmental neurons appear to directly target the M5 retinopetal neurons, while RMA neurons send their dendrites to the tectum and thereby receive retinotectal visual information (Vesselkin et al, , ). The M5 nucleus and RMA contain both glutamatergic and gamma‐aminobutyric acid (GABA)ergic neurons, presumably involved in modulating, enhancing or reducing RGC responsiveness (Rio et al, , , ).…”

Section: Sensory Component: Lateral Eyesmentioning

confidence: 99%

The stepwise development of the lamprey visual system and its evolutionary implications

Suzuki

Grillner

2018

Biological Reviews

View full text Add to dashboard Cite

Lampreys, which represent the oldest group of living vertebrates (cyclostomes), show unique eye development. The lamprey larva has only eyespot-like immature eyes beneath a non-transparent skin, whereas after metamorphosis, the adult has well-developed image-forming camera eyes. To establish a functional visual system, well-organised visual centres as well as motor components (e.g. trunk muscles for locomotion) and interactions between them are needed. Here we review the available knowledge concerning the structure, function and development of the different parts of the lamprey visual system. The lamprey exhibits stepwise development of the visual system during its life cycle. In prolarvae and early larvae, the 'primary' retina does not have horizontal and amacrine cells, but does have photoreceptors, bipolar cells and ganglion cells. At this stage, the optic nerve projects mostly to the pretectum, where the dendrites of neurons in the nucleus of the medial longitudinal fasciculus (nMLF) appear to receive direct visual information and send motor outputs to the neck and trunk muscles. This simple neural circuit may generate negative phototaxis. Through the larval period, the lateral region of the retina grows again to form the 'secondary' retina and the topographic retinotectal projection of the optic nerve is formed, and at the same time, the extra-ocular muscles progressively develop. During metamorphosis, horizontal and amacrine cells differentiate for the first time, and the optic tectum expands and becomes laminated. The adult lamprey then has a sophisticated visual system for image-forming and visual decision-making. In the adult lamprey, the thalamic pathway (retina-thalamus-cortex/pallium) also transmits visual stimuli. Because the primary, simple light-detecting circuit in larval lamprey shares functional and developmental similarities with that of protochordates (amphioxus and tunicates), the visual development of the lamprey provides information regarding the evolutionary transition of the vertebrate visual system from the protochordate-type to the vertebrate-type.

show abstract

Dual innervation of the lamprey retina by GABAergic and glutamatergic retinopetal fibers

Cited by 10 publications

References 33 publications

Presence of glutamate, glycine, and γ‐aminobutyric acid in the retina of the larval sea lamprey: Comparative immunohistochemical study of classical neurotransmitters in larval and postmetamorphic retinas

Presence of glutamate, glycine, and γ‐aminobutyric acid in the retina of the larval sea lamprey: Comparative immunohistochemical study of classical neurotransmitters in larval and postmetamorphic retinas

Glutamatergic neuronal populations in the brainstem of the sea lamprey, Petromyzon marinus: An in situ hybridization and immunocytochemical study

The stepwise development of the lamprey visual system and its evolutionary implications

Contact Info

Product

Resources

About