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

Abstract

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.

Gene Expression Identifies Distinct Ascending Glutamatergic Pathways to Frequency-Organized Auditory Cortex in the Rat Brain

“…This expression pattern is consistent with a VGLUT2 protein-dense terminal field found within thalamic recipient layers of sensory cortex (Kaneko et al, 2002;Nahmani and Erisir, 2005;Graziano et al, 2008;Hackett and de la Mothe, 2009). However, recent studies find that type 1 glutamate transporter (VGLUT1) mRNA is coexpressed with VGLUT2 mRNA in a subset of MGBv neurons in rodents (Barroso-Chinea et al, 2007;.…”

“…2D,G). This resembles that seen in other auditory and sensory cortices (Nahmani and Erisir, 2005;Graziano et al, 2008;Hackett and de la Mothe, 2009) and suggests that VGLUT2 protein expression alone does not readily distinguish the thalamocortical pathways to frequency-organized fields, A1 versus cSRAF.…”

Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses

“…Recent studies have shown that the refinement of the climbing fiberPurkinje cell connection in the cerebellum is associated with pruning of somatic innervation (33). Synaptic terminals of Pr5 axons in the VPm selectively express vesicular glutamate transporter 2 (VGluT2), whereas those of corticothalamic axons express only VGluT1 (34). This allowed us to visualize Pr5 axon terminals by using VGluT2 immunostaining.…”

The Somatosensory Cortex ofreelerMutant Mice Shows Absent Layering But Intact Formation and Behavioral Activation of Columnar Somatotopic Maps

“…Mapping of lemniscal thalamic boutons shows meaningful remodeling of terminal fields in reeler barrel cortex We took advantage of the recently shown specificity of vGluT2-antibodies to reveal the distribution of lemniscal thalamic boutons in the sensory neocortex (Graziano et al, 2008). In wild type, the clear modular pattern of termination in layer IV was reminiscent of barrels, which receive the densest innervation from the VPM (Fig.…”