Differential Synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats

• Type of Material: Article
• Authors: Dinesh V. Raju, Emory University; Deep J. Shah, University of Georgia; Terrence M. Wright, Emory University; Randy A Hall, Emory University; Yoland Smith, Emory University
• Language: English
• Date: 2006-11-10
• Publisher: Wiley: 12 months
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2006 Wiley‐Liss, Inc.
• Final Published Version (URL): http://dx.crossref.org/10.1002%2Fcne.21099
• Title of Journal or Parent Work: Journal of Comparative Neurology
• ISSN: 0021-9967
• Volume: 499
• Issue: 2
• Start Page: 231
• End Page: 243
• Grant/Funding Information: This study was supported by grants from the NIH to Y. Smith and R.A. Hall, an NRSA to DV Raju, an NIH base grant to the Yerkes National Primate Research Center (RR 00165) and a W.M. Keck Foundation Award to R.A. Hall.
• Keywords: striatum; vGluT1; thalamus; vGluT2; immunocytochemistry

Abstract

The striatum is divided into two compartments named the patch (or striosome) and matrix. Although these two compartments can be differentiated by their neurochemical content or afferent and efferent projections, the synaptology of inputs to these striatal regions remains poorly characterized. Using the vesicular glutamate transporters vGluT1 and vGluT2, as markers of corticostriatal and thalamostriatal projections, respectively, we demonstrate a differential pattern of synaptic connections of these two pathways between the patch and matrix compartments. We also demonstrate that the majority of vGluT2-immunolableled axon terminals form axo-spinous synapses, suggesting that thalamic afferents, like corticostriatal inputs, terminate preferentially onto spines in the striatum. Within both compartments more than 90% of vGluT1-containing terminals formed axo-spinous synapses, whereas 87% of vGluT2-positive terminals within the patch innervated dendritic spines, but only 55% did so in the matrix. To further characterize the source of thalamic inputs that could account for the increase in axo-dendritic synapses in the matrix, we undertook an electron microscopic analysis of the synaptology of thalamostriatal afferents to the matrix compartments from specific intralaminar, midline, relay, and associative thalamic nuclei in rats. Approximately 95% of PHA-L-labeled terminals from the central lateral, midline, mediodorsal, lateral dorsal, anteroventral and ventral anterior/ventral lateral nuclei formed axo-spinous synapses, a pattern reminiscent of corticostriatal afferents, but strikingly different from thalamostriatal projections arising from the parafascicular nucleus (PF), which terminate onto dendritic shafts. These findings provide the first evidence for a differential pattern of synaptic organization of thalamostriatal glutamatergic inputs to the patch and matrix compartments. Furthermore, they demonstrate that the PF is the sole source of significant axo-dendritic thalamic inputs to striatal projection neurons. These observations pave the way for understanding differential regulatory mechanisms of striatal outflow from the patch and matrix compartments by thalamostriatal afferents.