Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse

The ventral posterior nucleus of the thalamus (VP) receives two major sets of excitatory inputs, one from the ascending somatosensory pathways originating in the dorsal horn, dorsal column nuclei, and trigeminal nuclei, and the other originating from the cerebral cortex. Both systems use glutamate a...

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Bibliographic Details
Published in:Journal of comparative neurology (1911) 2008-03, Vol.507 (2), p.1258-1276
Main Authors: Graziano, Alessandro, Liu, Xiao-Bo, Murray, Karl D., Jones, Edward G.
Format: Article
Language:English
Subjects:
Afferent Pathways - metabolism
Afferent Pathways - ultrastructure
Animals
Biomarkers - analysis
Biomarkers - metabolism
BNPI
Brain Mapping - methods
Brain Stem - metabolism
Brain Stem - ultrastructure
core-matrix
corticothalamic
DNPI
Efferent Pathways - metabolism
Efferent Pathways - ultrastructure
Gene Expression - physiology
Glutamic Acid - metabolism
In Situ Hybridization
medial lemniscus
Mice
Microscopy, Confocal
Microscopy, Immunoelectron
Presynaptic Terminals - metabolism
Presynaptic Terminals - ultrastructure
RNA, Messenger - analysis
RNA, Messenger - metabolism
Somatosensory Cortex - metabolism
Somatosensory Cortex - ultrastructure
Spinal Cord - metabolism
Spinal Cord - ultrastructure
spinothalamic
synapses
Synaptic Transmission - physiology
Ventral Thalamic Nuclei - metabolism
Ventral Thalamic Nuclei - ultrastructure
Vesicular Glutamate Transport Protein 1 - genetics
Vesicular Glutamate Transport Protein 1 - metabolism
Vesicular Glutamate Transport Protein 2 - genetics
Vesicular Glutamate Transport Protein 2 - metabolism
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Summary:The ventral posterior nucleus of the thalamus (VP) receives two major sets of excitatory inputs, one from the ascending somatosensory pathways originating in the dorsal horn, dorsal column nuclei, and trigeminal nuclei, and the other originating from the cerebral cortex. Both systems use glutamate as neurotransmitter, as do the thalamocortical axons relaying somatosensory information from the VP to the primary somatosensory cortex (SI). The synapses formed by these projection systems differ anatomically, physiologically, and in their capacity for short‐term synaptic plasticity. Glutamate uptake into synaptic vesicles and its release at central synapses depend on two isoforms of vesicular glutamate transporters, VGluT1 and VGluT2. Despite ample evidence of their complementary distribution, some instances exist of co‐localization in the same brain areas or at the same synapses. In the thalamus, the two transcripts coexist in cells of the VP and other nuclei but not in the posterior or intralaminar nuclei. We show that the two isoforms are completely segregated at VP synapses, despite their widespread expression throughout the dorsal and ventral thalamus. We present immunocytochemical, ultrastructural, gene expression, and connectional evidence that VGluT1 in the VP is only found at corticothalamic synapses, whereas VGluT2 is only found at terminals made by axons originating in the spinal cord and brainstem. By contrast, the two VGluT isoforms are co‐localized in thalamocortical axon terminals targeting layer IV, but not in those targeting layer I, suggesting the presence of two distinct projection systems related to the core/matrix pattern of organization of thalamocortical connectivity described in other mammals. J. Comp. Neurol. 507:1258–1276, 2008. © 2008 Wiley‐Liss, Inc.
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.21592