Abstract
Glutamate is the main excitatory neurotransmitter involved in spinal cord circuits in vertebrates, but in most groups the distribution of glutamatergic spinal neurons is still unknown. Lampreys have been extensively used as a model to investigate the neuronal circuits underlying locomotion. Glutamatergic circuits have been characterized on the basis of the excitatory responses elicited in postsynaptic neurons. However, the presence of glutamatergic neurochemical markers in spinal neurons has not been investigated. In this study, we report for the first time the expression of a vesicular glutamate transporter (VGLUT) in the spinal cord of the sea lamprey. We also study the distribution of glutamate in perikarya and fibers. The largest glutamatergic neurons found were the dorsal cells and caudal giant cells. Two additional VGLUT-positive gray matter populations, one dorsomedial consisting of small cells and another one lateral consisting of small and large cells were observed. Some cerebrospinal fluid-contacting cells also expressed VGLUT. In the white matter, some edge cells and some cells associated with giant axons (Müller and Mauthner axons) and the dorsolateral funiculus expressed VGLUT. Large lateral cells and the cells associated with reticulospinal axons are in a key position to receive descending inputs involved in the control of locomotion. We also compared the distribution of glutamate immunoreactivity with that of γ-aminobutyric acid (GABA) and glycine. Colocalization of glutamate and GABA or glycine was observed in some small spinal cells. These results confirm the glutamatergic nature of various neuronal populations, and reveal new small-celled glutamatergic populations, predicting that some glutamatergic neurons would exert complex actions on postsynaptic neurons.
Highlights
Since the 1970s, glutamate has been recognized as the major excitatory neurotransmitter in the central nervous system of vertebrates [1,2,3]
Glutamate is introduced from the extracellular medium to the neuron cytoplasm by an excitatory amino acid transporter (EAAT; common for glutamate and aspartate) and it is transported into the synaptic vesicles by vesicular glutamate transporters (VGLUTs) specific for this amino acid
Our results showed that glutamate is present in the glycine-ir edge cells during both the larval and adult periods. This fact suggests that glutamate and glycine are co-released by some edge cells, but if this is involved in functional modulation of edge cells synapses on target cells needs to be investigated. This neurochemical study reports for the first time the presence of a variety of glutamatergic cell populations distributed along the spinal cord and raises the number of known glutamatergic cell types by two: cerebrospinal fluid-contacting (CSFc) cells around the central canal, and white matter interneurons
Summary
Since the 1970s, glutamate has been recognized as the major excitatory neurotransmitter in the central nervous system of vertebrates [1,2,3]. Anatomical studies of the glutamatergic system in mammals depended on the use of antibodies raised against glutamate-protein conjugates [15,16]. The use of these antibodies to characterize glutamatergic neurons was often considered problematic, because glutamate is a metabolic molecule found in all cells and because staining of perikarya was somewhat inconsistent [17]. The new studies with in situ hybridization for vesicular glutamate transporters allowed identifying unequivocally glutamatergic neuronal perikarya, whereas immunohistochemistry with antibodies raised against these transporters have been useful to identify axons of glutamatergic cells they fail to stain the perikaryon [10,13]. The morphology of glutamatergic neurons of lamina I and II of the rat dorsal horn has been investigated in detail using combined physiological and immunohistochemical methods to characterize vesicular glutamate transporters in axons of neurobiotin-injected single cells [10,18,19]
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