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

Authors

  • Verona Villar-Cerviño,

    1. Departamento de Biología Celular y Ecología, Facultad de Biología, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
    2. Instituto de Neurociencias, Universidad Miguel Hernández, Sant Joan d'Alacant 03550, Spain
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  • Antón Barreiro-Iglesias,

    1. Departamento de Biología Celular y Ecología, Facultad de Biología, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
    2. Center for Neural Repair and Rehabilitation, Shriners Hospitals Pediatric Research Center, Temple University School of Medicine, Philadelphia, Pennsylvania 19140
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  • Blanca Fernández-lópez,

    1. Departamento de Biología Celular y Ecología, Facultad de Biología, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
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  • Sylvie Mazan,

    1. Développement et Evolution des Vertébrés, UMR7150 CNRS and Université Paris 6, Station Biologique, 29680 Roscoff, France
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  • María Celina Rodicio,

    1. Departamento de Biología Celular y Ecología, Facultad de Biología, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
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  • Ramón Anadón

    Corresponding author
    1. Departamento de Biología Celular y Ecología, Facultad de Biología, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
    • Departamento de Biología Celular y Ecología, Facultad de Biología, Campus Sur, Universidad de Santiago de Compostela, Santiago de Compostela 15782, Spain
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Abstract

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. J. Comp. Neurol. 521:522–557, 2013. © 2012 Wiley Periodicals, Inc.

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